Grey matter lesions in MS From histology to clinical implications

Prion

Volumn 7, Issue 1, 2013, Pages 20-27

  Calabrese, Massimiliano ^a   Favaretto, Alice ^a   Martini, Valeria ^a,b   Gallo, Paolo ^b  

^a UNIVERSITY HOSPITAL OF PADOVA   (Italy)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cognitive dysfunction; Cortical lesions; Multiple sclerosis; Physical disability

Indexed keywords

BRAIN CORTEX LESION; CEREBROSPINAL FLUID; COGNITIVE DEFECT; CONFERENCE PAPER; DIAGNOSTIC ACCURACY; GRAY MATTER; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; MULTIPLE SCLEROSIS; NEUROIMAGING; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PHENOTYPE;

COGNITIVE DYSFUNCTION; CORTICAL LESIONS; MULTIPLE SCLEROSIS; PHYSICAL DISABILITY;

ANIMALS; CEREBRAL CORTEX; COGNITION DISORDERS; HUMANS; MAGNETIC RESONANCE IMAGING; MULTIPLE SCLEROSIS;

EID: 84874592067     PISSN: 19336896     EISSN: 1933690X     Source Type: Journal    
DOI: 10.4161/pri.22580     Document Type: Conference Paper

References (78)

1. Pirko I, Lucchinetti CF, Sriram S, Bakshi R. Gray matter involvement in multiple sclerosis. Neurology 2007; 68:634-42; PMID:17325269; http://dx.doi.org/10.1212/01.wnl.0000250267.85698.7a.
2. Popescu BF, Lucchinetti CF. Meningeal and cortical grey matter pathology in multiple sclerosis. [Review]. BMC Neurol 2012; 12:11; PMID:22397318; http://dx.doi.org/10.1186/1471-2377-12-11.
3. Lucchinetti CF, Popescu BF, Bunyan RF, Moll NM, Roemer SF, Lassmann H, et al. Inflammatory cortical demyelination in early multiple sclerosis. N Engl J Med 2011; 365:2188-97; PMID:22150037; http://dx.doi.org/10.1056/NEJMoa1100648.
4. De Stefano N, Matthews PM, Filippi M, Agosta F, De Luca M, Bartolozzi ML, et al. Evidence of early cortical atrophy in MS: relevance to white matter changes and disability. Neurology 2003; 60:1157- 62; PMID:12682324; http://dx.doi.org/10.1212/01.WNL.0000055926.69643.03.
5. Chard DT, Griffin CM, Rashid W, Davies GR, Altmann DR, Kapoor R, et al. Progressive grey matter atrophy in clinically early relapsing-remitting multiple sclerosis. Mult Scler 2004; 10:387-91; PMID:15327034; http://dx.doi.org/10. 1191/1352458504ms1050oa.
6. Peterson JW, Bö L, Mörk SJ, Chang A, Trapp BD. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 2001; 50:389-400; PMID:11558796; http://dx.doi.org/10.1002/ana.1123.
7. Bø L, Vedeler CA, Nyland HI, Trapp BD, Mørk SJ. Subpial demyelination in the cerebral cortex of multiple sclerosis patients. J Neuropathol Exp Neurol 2003; 62:723-32; PMID:12901699.
8. Geurts JJ, Bö L, Roosendaal SD, Hazes T, Daniëls R, Barkhof F, et al. Extensive hippocampal demyelination in multiple sclerosis. J Neuropathol Exp Neurol 2007; 66:819-27; PMID:17805012; http://dx.doi.org/10.1097/nen. 0b013e3181461f54.
9. Papadopoulos D, Dukes S, Patel R, Nicholas R, Vora A, Reynolds R. Substantial archaeocortical atrophy and neuronal loss in multiple sclerosis. Brain Pathol 2009; 19:238-53; PMID:18492094; http://dx.doi.org/10.1111/j.1750- 3639.2008.00177.x.
10. Vercellino M, Plano F, Votta B, Mutani R, Giordana MT, Cavalla P. Grey matter pathology in multiple sclerosis. J Neuropathol Exp Neurol 2005; 64:1101- 7; PMID:16319720; http://dx.doi.org/10.1097/01.jnen.0000190067.20935.42.
11. Kutzelnigg A, Lucchinetti CF, Stadelmann C, Brück W, Rauschka H, Bergmann M, et al. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 2005; 128:2705-12; PMID:16230320; http://dx.doi.org/ 10.1093/brain/awh641.
12. Gilmore CP, Donaldson I, Bö L, Owens T, Lowe JS, Evangelou N. Regional variations in the extent and pattern of grey matter demyelination in multiple sclerosis: a comparison between the cerebral cortex, cerebellar cortex, deep grey matter nuclei and the spinal cord. J Neurol Neurosurg Psychiatry 2009; 80:182- 7; PMID:18829630; http://dx.doi.org/10.1136/jnnp.2008.148767.
13. Albert M, Antel J, Brück W, Stadelmann C. Extensive cortical remyelination in patients with chronic multiple sclerosis. Brain Pathol 2007; 17:129-38; PMID:17388943; http://dx.doi.org/10.1111/j.1750-3639.2006.00043.x.
14. Kutzelnigg A, Faber-Rod JC, Bauer J, Lucchinetti CF, Sorensen PS, Laursen H, et al. Widespread demyelination in the cerebellar cortex in multiple sclerosis. Brain Pathol 2007; 17:38-44; PMID:17493036; http://dx.doi.org/10. 1111/j.1750-3639.2006.00041.x.
15. Brownell B, Hughes JT. The distribution of plaques in the cerebrum in multiple sclerosis. J Neurol Neurosurg Psychiatry 1962; 25:315-20; PMID:14016083; http://dx.doi.org/10.1136/jnnp.25.4.315.
16. Lumsden CE. The neuropathology of multiple sclerosis. In: Vinken PJ, Brun GW, eds. Handbook of clinical neurology. Vol. 9. Amsterdam: Elsevier, 1970: 217-309.
17. Gilmore CP, Bö 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; PMID:16911477; http://dx.doi.org/10.1111/j.1750-3639.2006.00018.x.
18. Gilmore CP, DeLuca GC, Bö L, Owens T, Lowe J, Esiri MM, et al. Spinal cord neuronal pathology in multiple sclerosis. Brain Pathol 2009; 19:642-9; PMID:19170682; http://dx.doi.org/10.1111/j.1750-3639.2008.00228.x.
19. Bö L, Geurts JJ, 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; PMID:17210812; http://dx.doi.org/10.1001/archneur.64.1.76.
20. Magliozzi R, Howell O, Vora A, Serafini B, Nicholas R, Puopolo M, et al. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain 2007; 130:1089-104; PMID:17438020; http://dx.doi.org/10.1093/brain/awm038.
21. Magliozzi R, Howell OW, Reeves C, Roncaroli F, Nicholas R, Serafini B, et al. A Gradient of neuronal loss and meningeal inflammation in multiple sclerosis. Ann Neurol 2010; 68:477-93; PMID:20976767; http://dx.doi.org/10.1002/ ana.22230.
22. Howell OW, Reeves CA, Nicholas R, Carassiti D, Radotra B, Gentleman SM, et al. Meningeal inflammation is widespread and linked to cortical pathology in multiple sclerosis. Brain 2011; 134:2755-71; PMID:21840891; http://dx.doi.org/ 10.1093/brain/awr182.
23. van Horssen J, Brink BP, de Vries HE, van der Valk P, Bø L. The blood-brain barrier in cortical multiple sclerosis lesions. J Neuropathol Exp Neurol 2007; 66:321- 8; PMID:17413323; http://dx.doi.org/10.1097/nen. 0b013e318040b2de.
24. Brink BP, Veerhuis R, Breij ECW, van der Valk P, Dijkstra CD, Bö L. The pathology of multiple sclerosis is location-dependent: no significant complement activation is detected in purely cortical lesions. J Neuropathol Exp Neurol 2005; 64:147-55; PMID:15751229.
25. Peterson JW, Bö L, Mörk S, Chang A, Ransohoff RM, Trapp BD. VCAM-1-positive microglia target oligodendrocytes at the border of multiple sclerosis lesions. J Neuropathol Exp Neurol 2002; 61:539-46; PMID:12071637.
26. Gray E, Thomas TL, Betmouni S, Scolding N, Love S. Elevated activity and microglial expression of myeloperoxidase in demyelinated cerebral cortex in multiple sclerosis. Brain Pathol 2008; 18:86-95; PMID:18042261; http://dx.doi.org/10.1111/j.1750-3639.2007.00110.x.
27. Dal Bianco A, Bradl M, Frischer J, Kutzelnigg A, Jellinger K, Lassmann H. Multiple sclerosis and Alzheimer's disease. Ann Neurol 2008; 63:174- 83; PMID:17924575; http://dx.doi.org/10.1002/ana.21240.
28. Dutta R, McDonough J, Yin X, Peterson J, Chang A, Torres T, et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 2006; 59:478-89; PMID:16392116; http://dx.doi.org/10.1002/ana.20736.
29. Haider L, Fischer MT, Frischer JM, Bauer J, Höftberger R, Botond G, et al. Oxidative damage in multiple sclerosis lesions. Brain 2011; 134:1914-24; PMID:21653539; http://dx.doi.org/10.1093/brain/awr128.
30. Gawne-Cain ML, O'Riordan JI, Thompson AJ, Moseley IF, Miller DH. Multiple sclerosis lesion detection in the brain: a comparison of fast fluid-attenuated inversion recovery and conventional T2-weighted dual spin echo. Neurology 1997; 49:364-70; PMID:9270563; http://dx.doi.org/10.1212/WNL.49.2.364.
31. Bakshi R, Ariyaratana S, Benedict RHB, Jacobs L. Fluid-attenuated inversion recovery magnetic resonance imaging detects cortical and juxtacortical multiple sclerosis lesions. Arch Neurol 2001; 58:742-8; PMID:11346369; http://dx.doi.org/10.1001/archneur. 58.5.742.
32. Geurts JJ, Bö L, Pouwels PJ, Castelijns JA, Polman CH, Barkhof F. Cortical lesions in multiple sclerosis: combined postmortem MR imaging and histopathology. AJNR Am J Neuroradiol 2005; 26:572-7; PMID:15760868.
33. Geurts JJ, Pouwels PJ, Uitdehaag BM, Polman CH, Barkhof F, Castelijns JA. Intracortical lesions in multiple sclerosis: improved detection with 3D double inversion-recovery MR imaging. Radiology 2005; 236:254-60; PMID:15987979; http://dx.doi.org/10.1148/radiol.2361040450.
34. Pouwels PJ, Kuijer JP, Mugler JP 3rd, Guttmann CR, Barkhof F. Human gray matter: feasibility of single-slab 3D double inversion-recovery high-spatialresolution MR imaging. Radiology 2006; 241:873-9; PMID:17053197; http://dx.doi.org/10.1148/radiol.2413051182.
35. Seewann A, Kooi EJ, Roosendaal SD, Pouwels PJ, Wattjes MP, van der Valk P, et al. Postmortem verification of MS cortical lesion detection with 3D DIR. Neurology 2012; 78:302-8; PMID:22218278; http://dx.doi.org/10.1212/WNL. 0b013e31824528a0.
36. Seewann A, Vrenken H, Kooi EJ, van der Valk P, Knol DL, Polman CH, et al. Imaging the tip of the iceberg: visualization of cortical lesions in multiple sclerosis. Mult Scler 2011; 17:1202-10; PMID:21561955; http://dx.doi.org/10. 1177/1352458511406575.
37. Nelson F, Poonawalla AH, Hou P, Huang F, Wolinsky JS, Narayana PA. 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; 28:1645-9; PMID:17885241; http://dx.doi.org/10.3174/ajnr.A0645.
38. Sethi V, Yousry TA, Muhlert N, Ron M, Golay X, Wheeler-Kingshott C, et al. Improved detection of cortical MS lesions with phase-sensitive inversion recovery MRI. J Neurol Neurosurg Psychiatry 2012; 83:877-82; PMID:22807559; http://dx.doi.org/10.1136/jnnp-2012-303023.
39. Nelson F, Poonawalla A, Hou P, Wolinsky JS, Narayana PA. 3D MPRAGE improves classification of cortical lesions in multiple sclerosis. Mult Scler 2008; 14:1214-9; PMID:18952832; http://dx.doi.org/10.1177/1352458508094644.
40. Calabrese M, De Stefano N, Atzori M, Bernardi V, Mattisi I, Barachino L, 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; PMID:17923625; http://dx.doi.org/10.1001/archneur.64.10.1416.
41. 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; PMID:20373349.
42. Calabrese M, Federle L, Bernardi V, Rinaldi F, Favaretto A, Varagnolo MC, et al. The association of intrathecal immunoglobulin synthesis and cortical lesions predicts disease activity in clinically isolated syndrome and early relapsing-remitting multiple sclerosis. Mult Scler 2012; 18:174-80; PMID:21868488; http://dx.doi.org/10.1177/1352458511418550.
43. Calabrese M, Rocca MA, Atzori M, Mattisi I, Bernardi V, Favaretto A, et al. Cortical lesions in primary progressive multiple sclerosis: a 2-year longitudinal MR study. Neurology 2009; 72:1330-6; PMID:19365054; http://dx.doi.org/10.1212/WNL.0b013e3181a0fee5.
44. Calabrese M, Battaglini M, Giorgio A, Atzori M, Bernardi V, Mattisi I, et al. Imaging distribution and frequency of cortical lesions in patients with multiple sclerosis. Neurology 2010; 75:1234-40; PMID:20739644; http://dx.doi.org/10.1212/WNL.0b013e3181f5d4da.
45. Rovaris M, Barkhof F, Calabrese M, De Stefano N, Fazekas F, Miller DH, et al. MRI features of benign multiple sclerosis: toward a new definition of this disease phenotype. Neurology 2009; 72:1693- 701; PMID:19433744; http://dx.doi.org/10.1212/WNL.0b013e3181a55feb.
46. Calabrese M, Filippi M, Rovaris M, Bernardi V, Atzori M, Mattisi I, et al. Evidence for relative cortical sparing in benign multiple sclerosis: a longitudinal magnetic resonance imaging study. Mult Scler 2009; 15:36-41; PMID:18755823; http://dx.doi.org/10.1177/1352458508096686.
47. Spatt J, Chaix R, Mamoli B. Epileptic and nonepileptic seizures in multiple sclerosis. J Neurol 2001; 248:2-9; PMID:11266015; http://dx.doi.org/10. 1007/s004150170262.
48. Engelsen BA, Grønning M. Epileptic seizures in patients with multiple sclerosis. Is the prognosis of epilepsy underestimated? Seizure 1997; 6:377-82; PMID:9663801; http://dx.doi.org/10.1016/S1059-1311(97)80037-4.
49. Calabrese M, De Stefano N, Atzori M, Bernardi V, Mattisi I, Barachino L, et al. Extensive cortical inflammation is associated with epilepsy in multiple sclerosis. J Neurol 2008; 255:581-6; PMID:18227989; http://dx.doi.org/10.1007/ s00415-008-0752-7.
50. Catenoix H, Marignier R, Ritleng C, Dufour M, Mauguière F, Confavreux C, et al. Multiple sclerosis and epileptic seizures. Mult Scler 2011; 17:96-102; PMID:20861180; http://dx.doi. org/10.1177/1352458510382246.
51. Calabrese M, Grossi P, Favaretto A, Romualdi C, Atzori M, Rinaldi F, et al. Cortical pathology in multiple sclerosis patients with epilepsy: a 3 year longitudinal study. J Neurol Neurosurg Psychiatry 2012; 83:49-54; PMID:21890577; http://dx.doi.org/10.1136/jnnp-2011-300414.
52. Absinta M, Rocca MA, Moiola L, Copetti M, Milani N, Falini A, et al. Cortical lesions in children with multiple sclerosis. Neurology 2011; 76:910- 3; PMID:21383327; http://dx.doi.org/10.1212/WNL.0b013e31820f2e69.
53. Calabrese M, Seppi D, Romualdi C, Rinaldi F, Alessio S, Perini P, et al. Gray matter pathology in MS: a 3-year longitudinal study in a pediatric population. AJNR Am J Neuroradiol 2012; 33:1507-11; PMID:22422186; http://dx.doi.org/10.3174/ajnr.A3011.
54. Popescu BF, Bunyan RF, Parisi JE, Ransohoff RM, Lucchinetti CF. A case of multiple sclerosis presenting with inflammatory cortical demyelination. Neurology 2011; 76:1705-10; PMID:21576686; http://dx.doi.org/10.1212/WNL. 0b013e31821a44f1.
55. Calabrese M, Gallo P. Magnetic resonance evidence of cortical onset of multiple sclerosis. Mult Scler 2009; 15:933-41; PMID:19667021; http://dx.doi.org/10.1177/1352458509106510.
56. Giorgio A, Stromillo ML, Rossi F, Battaglini M, Hakiki B, Portaccio E, et al. Cortical lesions in radiologically isolated syndrome. Neurology 2011; 77:1896- 9; PMID:22076541; http://dx.doi.org/10.1212/WNL.0b013e318238ee9b.
57. Filippi M, Rocca MA, Calabrese M, Sormani MP, Rinaldi F, Perini P, et al. Intracortical lesions: relevance for new MRI diagnostic criteria for multiple sclerosis. Neurology 2010; 75:1988-94; PMID:21115953; http://dx.doi.org/10.1212/ WNL.0b013e3181ff96f6.
58. McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD, et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 2001; 50:121-7; PMID:11456302; http://dx.doi.org/10.1002/ana.1032.
59. Polman CH, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann Neurol 2005; 58:840-6; PMID:16283615; http://dx.doi.org/10. 1002/ana.20703.
60. Swanton JK, Fernando K, Dalton CM, Miszkiel KA, Thompson AJ, Plant GT, et al. Modification of MRI criteria for multiple sclerosis in patients with clinically isolated syndromes. J Neurol Neurosurg Psychiatry 2006; 77:830-3; PMID:16043456; http://dx.doi.org/10.1136/jnnp.2005.073247.
61. Cotton F, Rambaud L, Hermier M. Dual inversion recovery MRI helps identifying cortical tubers in tuberous sclerosis. Epilepsia 2006; 47:1072-3; PMID:16822256; http://dx.doi.org/10.1111/j.1528-1167.2006.00529.x.
62. Rugg-Gunn FJ, Boulby PA, Symms MR, Barker GJ, Duncan JS. Imaging the neocortex in epilepsy with double inversion recovery imaging. Neuroimage 2006; 31:39-50; PMID:16460962; http://dx.doi.org/10.1016/j.neuroimage.2005.11.034.
63. Grant PE, Barkovich AJ, Wald LL, Dillon WP, Laxer KD, Vigneron DB. High-resolution surface-coil MR of cortical lesions in medically refractory epilepsy: a prospective study. AJNR Am J Neuroradiol 1997; 18:291-301; PMID:9111666.
64. Matsusue E, Kinoshita T, Ohama E, Ogawa T. Cerebral cortical and white matter lesions in chronic hepatic encephalopathy: MR-pathologic correlations. AJNR Am J Neuroradiol 2005; 26:347-51; PMID:15709133.
65. Turetschek K, Wunderbaldinger P, Bankier AA, Zontsich T, Graf O, Mallek R, et al. Double inversion recovery imaging of the brain: initial experience and comparison with fluid attenuated inversion recovery imaging. Magn Reson Imaging 1998; 16:127-35; PMID:9508269; http://dx.doi.org/10.1016/S0730-725X(97)00254-3.
66. Popescu BF, Parisi JE, Cabrera-Gómez JA, Newell K, Mandler RN, Pittock SJ, et al. Absence of cortical demyelination in neuromyelitis optica. Neurology 2010; 75:2103-9; PMID:21135384; http://dx.doi.org/10.1212/WNL. 0b013e318200d80c.
67. Calabrese M, Oh MS, Favaretto A, Rinaldi F, Poretto V, Alessio S, et al. No MRI evidence of cortical lesions in neuromyelitis optica. Neurology 2012; 79:1671- 6; PMID:22993282; http://dx.doi.org/10.1212/WNL.0b013e31826e9a96.
68. Absinta M, Rocca MA, Colombo B, Copetti M, De Feo D, Falini A, et al. Patients with migraine do not have MRI-visible cortical lesions. J Neurol 2012; In Press; PMID:22714135; http://dx.doi.org/10.1007/s00415-012-6571-x.
69. Amato MP, Zipoli V, Portaccio E. Multiple sclerosisrelated cognitive changes: a review of cross-sectional and longitudinal studies. J Neurol Sci 2006; 245:41- 6; PMID:16643953; http://dx.doi.org/10.1016/j.jns.2005.08.019.
70. Rovaris M, Filippi M, Minicucci L, Iannucci G, Santuccio G, Possa F, et al. Cortical/subcortical disease burden and cognitive impairment in patients with multiple sclerosis. AJNR Am J Neuroradiol 2000; 21:402-8; PMID:10696031.
71. Rao SM, Leo GJ, Haughton VM, St Aubin-Faubert P, Bernardin L. Correlation of magnetic resonance imaging with neuropsychological testing in multiple sclerosis. Neurology 1989; 39:161-6; PMID:2915783; http://dx.doi.org/10.1212/ WNL.39.2.161.
72. 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; 61:226-30; PMID:14967771; http://dx.doi.org/10.1001/ archneur.61.2.226.
73. Portaccio E, Amato MP, Bartolozzi ML, Zipoli V, Mortilla M, Guidi L, et al. Neocortical volume decrease in relapsing-remitting multiple sclerosis with mild cognitive impairment. J Neurol Sci 2006; 245:195- 9; PMID:16631794; http://dx.doi.org/10.1016/j.jns.2005.07.019.
74. Benedict RH, Bruce JM, Dwyer MG, Abdelrahman N, Hussein S, Weinstock-Guttman B, et al. Neocortical atrophy, third ventricular width, and cognitive dysfunction in multiple sclerosis. Arch Neurol 2006; 63:1301- 6; PMID:16966509; http://dx.doi.org/10.1001/archneur.63.9.1301.
75. Tekok-Kilic A, Benedict RH, Weinstock-Guttman B, Dwyer MG, Carone D, Srinivasaraghavan B, et al. Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis. Neuroimage 2007; 36:1294-300; PMID:17524670; http://dx.doi.org/10.1016/j.neuroimage.2007.04.017.
76. Morgen K, Sammer G, Courtney SM, Wolters T, Melchior H, Blecker CR, et al. Evidence for a direct association between cortical atrophy and cognitive impairment in relapsing-remitting MS. Neuroimage 2006; 30:891-8; PMID:16360321; http://dx.doi. org/10.1016/j.neuroimage.2005.10.032.
77. 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; PMID:19752305; http://dx.doi.org/10.1001/archneurol.2009.174.
78. Roosendaal SD, Moraal B, Pouwels PJ, Vrenken H, Castelijns JA, Barkhof F, et al. Accumulation of cortical lesions in MS: relation with cognitive impairment. Mult Scler 2009; 15:708-14; PMID:19435749; http://dx.doi.org/10. 1177/1352458509102907.