The neuropathological basis of clinical progression in multiple sclerosis

Acta Neuropathologica

Volumn 122, Issue 2, 2011, Pages 155-170

  Reynolds, Richard ^a   Roncaroli, Federico ^a   Nicholas, Richard ^a   Radotra, Bishan ^a   Gveric, Djordje ^a   Howell, Owain ^a  

^a Centre for Neuroscience   (United Kingdom)

Author keywords

Axon loss; Clinical progression; Demyelination; Inflammation; Neurodegeneration; Remyelination

Indexed keywords

AMYLOID PRECURSOR PROTEIN; GADOLINIUM PENTETATE; GLUTAMIC ACID; N ACETYLASPARTIC ACID;

ALLERGIC ENCEPHALOMYELITIS; BRAIN ATROPHY; CELL INFILTRATION; DEMYELINATION; DISEASE COURSE; DISEASE DURATION; GENE DELETION; GRAY MATTER; HEALTH CARE FACILITY; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFLAMMATION; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NEUROIMAGING; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; REMYELINIZATION; REVIEW; WHITE MATTER;

BRAIN; DEMYELINATING DISEASES; DISEASE PROGRESSION; HUMANS; INFLAMMATION; MULTIPLE SCLEROSIS; NERVE DEGENERATION;

EID: 79960835277     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-011-0840-0     Document Type: Review

References (86)

1. IV Allen SR McKeown 1979 A histological, histochemical and biochemical study of the macroscopically normal white matter in multiple sclerosis J Neurol Sci 41 81 91 438845 10.1016/0022-510X(79)90142-4 1:STN:280:DyaE1M7nsVOitQ%3D%3D (Pubitemid 9083274)
2. H Babbe A Roers A Waisman, et al. 2000 Clonal expansions of CD8(+) T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction J Exp Med 192 393 404 10934227 10.1084/jem.192.3.393 1:CAS:528:DC%2BD3cXlsFygt7g%3D (Pubitemid 30629164)
3. MH Barnett JW Prineas 2004 Relapsing and remitting multiple sclerosis: pathology of a newly forming lesion Ann Neurol 55 458 468 15048884 10.1002/ana.20016 (Pubitemid 38391962)
4. C Bjartmar G Kidd S Mörk, et al. 2000 Neurological disability correlates with spinal cord axonal loss and reduced N-acetyl aspartate in chronic multiple sclerosis patients Ann Neurol 48 893 901 11117546 10.1002/1531-8249(200012)48:6<893::AID-ANA10>3.0.CO;2-B 1:CAS:528:DC%2BD3MXhtlKqsw%3D%3D
5. L Bö CA Vedeler H Nyland BD Trapp SJ Mörk 2003 Intracortical multiple sclerosis lesions are not associated with increased lymphocyte infiltration Multiple Scler 4 323 331 10.1191/1352458503ms917oa (Pubitemid 36958014)
6. L Bö JJ Geurts R Ravid F Barkhof 2004 Magnetic resonance imaging as a tool to examine the neuropathology of multiple sclerosis Neuropathol Appl Neurobiol 30 106 117 15043708 10.1111/j.1365-2990.2003.00521.x (Pubitemid 38496701)
7. L Bö JJ Geurts SJ Mork P van der Valk 2006 Grey matter pathology in multiple sclerosis Acta Neurol Scand Suppl 183 48 50 16637929 10.1111/j.1600-0404.2006.00615.x
8. L Bö J Geurts P Van der Valk C Polman F Barkhof 2007 Lack of correlation between cortical demyelination and white matter pathologic changes in multiple sclerosis Arch Neurol 64 74 80 10.1001/archneur.64.1.76 (Pubitemid 46072427)
9. U Bonati LK Fisniku DR Altmann, et al. 2011 Cervical cord and brain grey matter atrophy independently associate with long term MS disability J Neurol Neurosurg Psychiatry 82 471 472 20710012 10.1136/jnnp.2010.205021 1:STN:280:DC%2BC3M3mslCqtA%3D%3D
10. J Booss MM Esiri WW Tourtellotte DY Mason 1983 Immunohistological analysis of T lymphocyte subsets in the central nervous system in chronic progressive multiple sclerosis J Neurol Sci 62 219 232 6607973 10.1016/0022-510X(83)90201-0 1:STN:280:DyaL2c7jslOjtQ%3D%3D (Pubitemid 14176251)
11. S Bramow JM Frischer H Lassmann, et al. 2010 Demyelination versus remyelination in progressive multiple sclerosis Brain 133 2983 2998 20855416 10.1093/brain/awq250
12. ECW Breij BP Brink R Veerhuis C van den Berg, et al. 2008 Homogeneity of active demyelinating lesions in established multiple sclerosis Ann Neurol 63 16 25 18232012 10.1002/ana.21311 1:CAS:528:DC%2BD1cXivF2itLw%3D (Pubitemid 351240547)
13. PA Brex O Ciccarelli JI O'Riordan, et al. 2002 A longitudinal study of abnormalities on MRI and disability from multiple sclerosis N Engl J Med 346 158 164 11796849 10.1056/NEJMoa011341 (Pubitemid 34438881)
14. W Brück P Porada S Poser, et al. 1995 Monocyte/macrophage differentiation in early multiple sclerosis lesions Ann Neurol 38 788 796 7486871 10.1002/ana.410380514
15. M Calabrese N de Stefano M Atzori, et al. 2007 Detection of cortical inflammatory lesions by double inversion recovery magnetic resonance imaging in patients with multiple sclerosis Arch Neurol 64 1416 1422 17923625 10.1001/archneur.64.10.1416 (Pubitemid 47572665)
16. M Calabrese N de Stefano M Atzori, et al. 2008 Extensive cortical inflammation is associated with epilepsy in multiple sclerosis J Neurol 255 581 586 18227989 10.1007/s00415-008-0752-7
17. M Calabrese MA Rocca M Atzori, et al. 2010 A 3-year magnetic resonance imaging study of cortical lesions in relapse-onset multiple sclerosis Ann Neurol 67 376 383 20373349
18. M Calabrese M Filippi P Gallo 2010 Cortical lesions in multiple sclerosis Nat Rev Neurol 6 438 444 20625376 10.1038/nrneurol.2010.93
19. GR Campbell I Ziabreva AK Reeve, et al. 2011 Mitochondrial DNA deletions and neurodegeneration in multiple sclerosis Ann Neurol 69 481 492 21446022 10.1002/ana.22109 1:CAS:528:DC%2BC3MXls1Omtbk%3D
20. A Cifelli M Arridge P Jezzard MM Esiri J Palace PM Matthews 2002 Thalamic neurodegeneration in multiple sclerosis Ann Neurol 52 650 653 12402265 10.1002/ana.10326 (Pubitemid 35246871)
21. RJ Clements J McDonough EJ Freeman 2008 Distribution of parvalbumin and calretinin immunoreactive interneurons in motor cortex from multiple sclerosis post-mortem tissue Exp Brain Res 187 459 465 18297277 10.1007/s00221-008-1317-9 1:CAS:528:DC%2BD1cXlsFyjs7c%3D
22. A Compston A Coles 2008 Multiple sclerosis Lancet 372 1502 1517 18970977 10.1016/S0140-6736(08)61620-7 1:CAS:528:DC%2BD1cXht12gtLvN
23. C Confavreux S Vukusic 2006 Age at disability milestones in multiple sclerosis Brain 129 595 605 16415309 10.1093/brain/awh714 (Pubitemid 43278222)
24. C Confavreux S Vukusic T Moreau P Adeleine 2000 Relapses and progression of disability in multiple sclerosis N Engl J Med 343 1430 1438 11078767 10.1056/NEJM200011163432001 1:STN:280:DC%2BD3M%2FisFWnsg%3D%3D
25. A Dal Bianco M Bradl J Frischer A Kutzelnigg K Jellinger H Lassmann 2008 Multiple sclerosis and Alzheimer's disease Ann Neurol 63 174 183 17924575 10.1002/ana.21240 (Pubitemid 351355296)
26. CJ de Groot E Bergers W Kamphorst, et al. 2001 Post-mortem MRI-guided sampling of multiple sclerosis brain lesions: increased yield of active demyelinating and (p)reactive lesions Brain 124 1635 1645 11459754 10.1093/brain/124.8.1635 (Pubitemid 32726776)
27. N De Stefano PM Matthews L Fu, et al. 1998 Axonal damage correlates with disability in patients with relapsing-remitting multiple sclerosis. Results of a longitudinal magnetic resonance spectroscopy study Brain 121 1469 1477 9712009 10.1093/brain/121.8.1469 (Pubitemid 28349900)
28. N de Stefano PM Matthews M Filippi, et al. 2003 Evidence of early cortical atrophy in MS: relevance to white matter changes and disability Neurology 60 1157 1162 12682324 (Pubitemid 36418778)
29. MS Deloire A Ruet D Hamel M Bonnet V Dousset B Brochet 2011 MRI predictors of cognitive outcome in early multiple sclerosis Neurology 76 1161 1167 21444901 10.1212/WNL.0b013e318212a8be 1:STN:280:DC%2BC3MzktFCnsg%3D%3D
30. R Dutta J McDonough X Yin, et al. 2006 Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients Ann Neurol 59 478 489 16392116 10.1002/ana.20736 1:CAS:528:DC%2BD28XjtV2ltr4%3D (Pubitemid 43358068)
31. R Dutta A Chang MK Doud, et al. 2011 Demyelination causes synaptic alterations in hippocampi from multiple sclerosis patients Ann Neurol 69 445 454 21446020 10.1002/ana.22337 1:CAS:528:DC%2BC3MXls1Omtb0%3D
32. N Evangelou MM Esiri S Smith, et al. 2000 Quantitative pathological evidence for axonal loss in normal appearing white matter in multiple sclerosis Ann Neurol 47 391 395 10716264 10.1002/1531-8249(200003)47:3<391::AID- ANA20>3.0.CO;2-J 1:STN:280:DC%2BD3c7nvFSjug%3D%3D (Pubitemid 30141854)
33. B Ferguson MK Matyszak MM Esiri VH Perry 1997 Axonal damage in acute multiple sclerosis lesions Brain 120 393 399 9126051 10.1093/brain/120.3.393 (Pubitemid 27153632)
34. M Filippi DW Paty L Kappos, et al. 1995 Correlations between changes in disability and T2-weighted brain MRI activity in multiple sclerosis: a follow-up study Neurology 45 255 260 7854522 1:STN:280:DyaK2M7lslOnsA%3D%3D
35. E Fisher JC Lee K Nakamura RA Rudick 2008 Gray matter atrophy in multiple sclerosis: a longitudinal study Ann Neurol 64 255 265 18661561 10.1002/ana.21436
36. LK Fisniku DT Chard JS Jackson, et al. 2008 Gray matter atrophy is related to long-term disability in multiple sclerosis Ann Neurol 64 247 254 18570297 10.1002/ana.21423
37. + T cells in multiple sclerosis Ann Neurol 66 132 141 19743458 10.1002/ana.21744 1:CAS:528: DC%2BD1MXht1ansrbJ
38. JM Frischer S Bramow A Dal-Bianco, et al. 2009 The relation between inflammation and neurodegeneration in multiple sclerosis brains Brain 132 1175 1189 19339255 10.1093/brain/awp070
39. L Fu PM Matthews N De Stefano 1998 Imaging axonal damage of normal-appearing white matter in multiple sclerosis Brain 121 103 113 9549491 10.1093/brain/121.1.103 (Pubitemid 28045509)
40. JJ Geurts PJ Pouwels BM Uitdehaag, et al. 2005 Intracortical lesions in multiple sclerosis: improved detection with 3D double inversion-recovery MR imaging Radiology 236 254 260 15987979 10.1148/radiol.2361040450 (Pubitemid 40853320)
41. JJ Geurts L Bo SD Roosendaal, et al. 2007 Extensive hippocampal demyelination in multiple sclerosis J Neuropathol Exp Neurol 66 819 827 17805012 10.1097/nen.0b013e3181461f54 (Pubitemid 47360957)
42. JJ Geurts F Barkhof 2008 Grey matter pathology in multiple sclerosis Lancet Neurol 7 841 851 18703006 10.1016/S1474-4422(08)70191-1
43. CP Gilmore I Donaldson L Bo T Owens J Lowe N Evangelou 2009 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 80 182 187 18829630 10.1136/jnnp.2008.148767 1:STN:280:DC%2BD1M%2Fnsleltg%3D%3D
44. A Giorgio N de Stefano 2010 Cognition in multiple sclerosis: relevance of lesions, brain atrophy and proton MR spectroscopy Neurol Sci 31 Suppl 2 S245 S248 20635111 10.1007/s10072-010-0370-x
45. SB Glad JH Aarseth H Nyland T Riise KM Myhr 2010 Benign multiple sclerosis: a need for a consensus Acta Neurol Scand Suppl 190 44 50 20586735 10.1111/j.1600-0404.2010.01375.x
46. A Guseo K Jellinger 1975 The significance of perivascular infiltrations in multiple sclerosis J Neurol 211 51 60 56431 10.1007/BF00312463 1:STN:280:DyaE287ksFChsA%3D%3D
47. S Hochmeister R Grundtner J Bauer, et al. 2006 Dysferlin is a new marker for leaky brain blood vessels in multiple sclerosis J Neuropathol Exp Neurol 65 855 865 16957579 10.1097/01.jnen.0000235119.52311.16 1:CAS:528: DC%2BD28XhtVGitrvN (Pubitemid 44371231)
48. OW Howell A Palser A Polito, et al. 2006 Disruption of neurofascin localisation reveals early changes preceding demyelination and remyelination in multiple sclerosis Brain 129 3173 3185 17041241 10.1093/brain/awl290 1:STN:280:DC%2BD28npsVyhsQ%3D%3D (Pubitemid 44871434)
49. OW Howell JL Rundle A Garg M Komada PJ Brophy R Reynolds 2010 Activated microglia mediate axoglial disruption that contributes to axonal injury in multiple sclerosis J Neuropathol Exp Neurol 69 1017 1033 20838243 10.1097/NEN.0b013e3181f3a5b1
50. B Kornek H Lassmann 1999 Axonal pathology in multiple sclerosis: a historical note Brain Pathol 9 651 656 10517504 10.1111/j.1750-3639.1999. tb00547.x 1:STN:280:DyaK1MvksFSqsA%3D%3D (Pubitemid 29470958)
51. M Kremenchutzky GP Rice J Baskerville DM Wingerchuk GC Ebers 2006 The natural history of multiple sclerosis: a geographically based study 9: observations on the progressive phase of the disease Brain 129 584 594 16401620 10.1093/brain/awh721 1:STN:280:DC%2BD28%2FovFymtw%3D%3D (Pubitemid 43278221)
52. T Kuhlmann G Lingfeld A Bitsch J Schuchardt W Bruck 2002 Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time Brain 125 2202 2212 12244078 10.1093/brain/awf235
53. A Kutzelnigg CF Lucchinetti C Stadelmann, et al. 2005 Cortical demyelination and diffuse white matter injury in multiple sclerosis Brain 128 2705 2712 16230320 10.1093/brain/awh641 (Pubitemid 41552953)
54. Lassmann H, Wekerle H (2005) The pathology of multiple sclerosis. McAlpine's multiple sclerosis, vol 4. Churchill Livingstone, London, pp 557-599
55. E Leray J Yaouanq E Le Page, et al. 2010 Evidence for a two-stage disability progression in multiple sclerosis Brain 133 1900 1913 20423930 10.1093/brain/awq076
56. NA Losseff SL Webb JI O'Riordan, et al. 1996 Spinal cord atrophy and disability in multiple sclerosis. A new reproducible and sensitive MRI method with potential to monitor disease progression Brain 119 2009 2019 9010005 10.1093/brain/119.6.2009 (Pubitemid 27032631)
57. G Lovas N Szilagyi K Majtenyi, et al. 2000 Axonal changes in chronic demyelinated cervical spinal cord plaques Brain 123 308 317 10648438 10.1093/brain/123.2.308 (Pubitemid 30055154)
58. C Lucchinetti W Bruck J Parisi B Scheithauer M Rodriguez H Lassmann 2000 Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination Ann Neurol 47 707 717 10852536 10.1002/1531-8249(200006)47: 6<707::AID-ANA3>3.0.CO;2-Q 1:STN:280:DC%2BD3czgvFektA%3D%3D (Pubitemid 30390191)
59. R Magliozzi O Howell A Vora, et al. 2007 Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology Brain 130 1089 1104 17438020 10.1093/brain/awm038 (Pubitemid 47355604)
60. R Magliozzi OW Howell C Reeves, et al. 2010 A Gradient of neuronal loss and meningeal inflammation in multiple sclerosis Ann Neurol 68 477 493 20976767 10.1002/ana.22230 1:CAS:528:DC%2BC3cXhsVOrur7I
61. D McAlpine 1961 The benign form of multiple sclerosis. A study based on 241 cases seen within three years of onset and followed up until the tenth year or more of the disease Brain 84 186 203 13773723 10.1093/brain/84.2.186 1:STN:280:DyaF3c%2Fptlyhtw%3D%3D
62. E Meinl M Krumholtz T Derfuss A Junker R Hohlfeld 2008 Compartmentalization of inflammation in the CNS: a major mechanism driving progressive multiple sclerosis J Neurol Sci 274 42 44 18715571 10.1016/j.jns.2008.06.032 1:CAS:528:DC%2BD1cXht1eitr3F
63. DH Miller 1995 Magnetic resonance imaging and spectroscopy in multiple sclerosis Curr Opin Neurol 8 210 215 7551120 10.1097/00019052-199506000-00009 1:STN:280:DyaK28%2Fitlygug%3D%3D
64. PD Molyneux M Filippi F Barkhof, et al. 1998 Correlations between monthly enhanced MRI lesion rate and changes in T2 lesion volume in multiple sclerosis Ann Neurol 43 332 339 9506550 10.1002/ana.410430311 1:STN:280: DyaK1c7msFektw%3D%3D (Pubitemid 28113596)
65. H Neumann I Medana J Bauer H Lassmann 2002 Cytotoxic T lymphocytes in autoimmune and degenerative CNS diseases Trend Neurosci 25 313 319 12086750 10.1016/S0166-2236(02)02154-9 1:CAS:528:DC%2BD38Xks1ymtLo%3D (Pubitemid 34667013)
66. GJ Nijeholt E Bergers W Kamphorst, et al. 2001 Post-mortem high-resolution MRI of the spinal cord in multiple sclerosis: a correlative study with conventional MRI, histopathology and clinical phenotype Brain 124 154 166 11133795 10.1093/brain/124.1.154 1:STN:280:DC%2BD3M7gvV2isQ%3D%3D (Pubitemid 32055997)
67. R Patani M Balaratnam A Vora R Reynolds 2007 Remyelination can be extensive in multiple sclerosis despite a long disease course Neuropath App Neurobiol 33 277 287 10.1111/j.1365-2990.2007.00805.x 1:CAS:528: DC%2BD2sXnsVSgu74%3D (Pubitemid 46701044)
68. P Patrikios C Stadelmann A Kutzelnigg, et al. 2006 Remyelination is extensive in a subset of multiple sclerosis patients Brain 129 3165 3172 16921173 10.1093/brain/awl217 (Pubitemid 44871433)
69. JW Peterson L Bö S Mörk A Chang BD Trapp 2001 Transected neuritis, apoptotic neurons and reduced inflammation in cortical multiple sclerosis lesions Ann Neurol 50 389 400 11558796 10.1002/ana.1123 1:STN:280:DC%2BD3MrhtFCnug%3D%3D (Pubitemid 32848742)
70. I Pirko CF Lucchinetti S Sriram R Bakshi 2007 Gray matter involvement in multiple sclerosis Neurology. 68 634 642 17325269 10.1212/01.wnl.0000250267. 85698.7a (Pubitemid 46667808)
71. JW Prineas RO Barnard T Revesz EE Kwon L Sharer ES Cho 1993 Multiple sclerosis. Pathology of recurrent lesions Brain 116 681 693 8513397 10.1093/brain/116.3.681 (Pubitemid 23203644)
72. M Rovaris F Barkhof M Calabrese, et al. 2009 MRI features of benign multiple sclerosis: toward a new definition of this disease phenotype Neurology 72 1693 1701 19433744 10.1212/WNL.0b013e3181a55feb 1:STN:280: DC%2BD1MzjslOgug%3D%3D
73. A Scalfari A Neuhaus A Degenhardt, et al. 2010 The natural history of multiple sclerosis: a geographically based study 10: relapses and long-term disability Brain 133 1914 1929 20534650 10.1093/brain/awq118
74. A Seewann EJ Kooi SD Roosendaal F Barkhof P van der Valk JJ Geurts 2009 Translating pathology in multiple sclerosis: the combination of post-mortem imaging, histopathology and clinical findings Acta Neurol Scand 119 349 355 19254283 10.1111/j.1600-0404.2008.01137.x 1:STN:280:DC%2BD1MzntlWmtg%3D%3D
75. K Schmierer F Scaravilli DR Altmann GJ Barker DH Miller 2004 Magnetization transfer ratio and myelin in post-mortem multiple sclerosis brain Ann Neurol 56 407 415 15349868 10.1002/ana.20202 (Pubitemid 39166560)
76. K Schmierer HG Parkes P-W So, et al. 2010 High field (9.4 Tesla) magnetic resonance imaging of cortical grey matter lesions in multiple sclerosis Brain 133 858 867 20123726 10.1093/brain/awp335
77. V Siffrin J Vogt H Radbruch R Nitsch F Zipp 2010 Multiple sclerosis-candidate mechanisms underlying CNS atrophy Trends Neurosci 33 202 210 20153532 10.1016/j.tins.2010.01.002 1:CAS:528:DC%2BC3cXksVejs7s%3D
78. KJ Smith R Kapoor SM Hall M Davies 2001 Electrically active axons degenerate when exposed to nitric oxide Ann Neurol 49 470 479 11310624 10.1002/ana.96 1:CAS:528:DC%2BD3MXjtVyjtL0%3D (Pubitemid 32281330)
79. Stadelmann C (2011) Multiple sclerosis as a neurodegenerative disease: pathology, mechanisms and therapeutic implications. Curr Opin Neurol Adv. Access Mar 31
80. BD Trapp J Peterson RM Ransohoff R Rudick S Mörk L Bö 1998 Axonal transection in the lesions of multiple sclerosis N Engl J Med 338 278 285 9445407 10.1056/NEJM199801293380502 1:STN:280:DyaK1c%2Fpt1SksA%3D%3D (Pubitemid 28065253)
81. P Van der Valk S Amor 2009 Preactive lesions in multiple sclerosis Curr Opin Neurol 22 207 213 19417567
82. MM Vellinga RD Oude Engberink A Seewann, et al. 2008 Pluriformity of inflammation in multiple sclerosis shown by ultra-small iron oxide particle enhancement Brain 131 800 807 18245785 10.1093/brain/awn009 (Pubitemid 351294725)
83. M Vercellino F Plano B Votta R Mutani MT Giordana P Cavalla 2005 Grey matter pathology in multiple sclerosis J Neuropathol Exp Neurol 64 1101 1107 16319720 10.1097/01.jnen.0000190067.20935.42
84. O Vuia 1977 The benign form of multiple sclerosis. Anatomo-clinical aspects Acta Neurol Scand 55 289 298 857573 10.1111/j.1600-0404.1977.tb05648.x 1:STN:280:DyaE2s7nvVejsQ%3D%3D (Pubitemid 8062309)
85. C Wegner MM Esiri SA Chance J Palace PM Matthews 2006 Neocortical neuronal, synaptic, and glial loss in multiple sclerosis Neurology 67 960 967 17000961 10.1212/01.wnl.0000237551.26858.39 1:STN:280:DC%2BD28rnt1SitA%3D%3D (Pubitemid 44454585)
86. J Wuerfel M Haertle H Waiczies, et al. 2008 Perivascular spaces-MRI marker of inflammatory activity in the brain? Brain 131 2332 2340 18676439 10.1093/brain/awn171