The role of advanced magnetic resonance imaging techniques in primary progressive MS

Journal of Neurology

Volumn 259, Issue 4, 2012, Pages 611-621

  Rocca, Maria A ^a   Absinta, Martina ^a   Filippi, Massimo ^a  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

1H MRS; DT MRI; FMRI; MRI; MT MRI; Primary progressive multiple sclerosis

Indexed keywords

GADOLINIUM;

BOLD SIGNAL; BRAIN ATROPHY; BRAIN DAMAGE; BRAIN TISSUE; CENTRAL NERVOUS SYSTEM DISEASE; CERVICAL SPINAL CORD; CLINICAL FEATURE; COGNITION; CONTRAST ENHANCEMENT; DEMYELINATION; DIAGNOSTIC VALUE; DIFFUSION TENSOR IMAGING; DIFFUSION WEIGHTED IMAGING; DISABILITY; DISEASE SEVERITY; FRACTIONAL ANISOTROPY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; LONGITUDINAL STUDY; MOVEMENT (PHYSIOLOGY); MULTICENTER STUDY (TOPIC); MULTIPLE SCLEROSIS; NEUROIMAGING; NEUROPATHOLOGY; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PRIMARY PROGRESSIVE MULTIPLE SCLEROSIS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; RISK FACTOR; SENSITIVITY AND SPECIFICITY; SPINAL CORD ATROPHY; SYMPTOM; TASK PERFORMANCE; TOPOGRAPHY; VOXEL BASED MORPHOMETRY; WHITE MATTER LESION;

BRAIN; HUMANS; MAGNETIC RESONANCE IMAGING; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; SPINAL CORD;

EID: 84862520343     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-011-6195-6     Document Type: Review

References (79)

1. Agosta F, Benedetti B, Rocca MA, Valsasina P, Rovaris M, Comi G, Filippi M (2005) Quantification of cervical cord pathology in primary progressive MS using diffusion tensor MRI. Neurology 64:631-635 (Pubitemid 40261890)
2. Agosta F, Absinta M, Sormani MP, Ghezzi A, Bertolotto A, Montanari E, Comi G, Filippi M (2007) In vivo assessment of cervical cord damage in MS patients: a longitudinal diffusion tensor MRI study. Brain 130:2211-2219 (Pubitemid 47236613)
3. Agosta F, Valsasina P, Absinta M, Sala S, Caputo D, Filippi M (2009) Primary progressive multiple sclerosis: tactile-associated functional MR activity in the cervical spinal cord. Radiology 253:209-215
4. Anderson VM, Fisniku LK, Khaleeli Z, Summers MM, Penny SA, Altmann DR, Thompson AJ, Ron MA, Miller DH (2010) Hippocampal atrophy in relapsing-remitting and primary progressive MS: a comparative study. Mult Scler 16:1083-1090
5. Bakshi R, Thompson AJ, Rocca MA, Pelletier D, Dousset V, Barkhof F, Inglese M, Guttmann CR, Horsfield MA, Filippi M (2008) MRI in multiple sclerosis: current status and future prospects. Lancet Neurol 7:615-625
6. Barkhof F, Bruck W, De Groot CJ, Bergers E, Hulshof S, Geurts J, Polman CH, van der Valk P (2003) Remyelinated lesions in multiple sclerosis: magnetic resonance image appearance. Arch Neurol 60:1073-1081 (Pubitemid 36975794)
7. Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66:259-267 (Pubitemid 24016507)
8. Bodini B, Khaleeli Z, Cercignani M, Miller DH, Thompson AJ, Ciccarelli O (2009) 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 30:2852-2861
9. Bodini B, Battaglini M, De Stefano N, Khaleeli Z, Barkhof F, Chard D, Filippi M, Montalban X, Polman C, Rovaris M, Rovira A, Samson R, Miller D, Thompson A, Ciccarelli O (2011) T2 lesion location really matters: a 10 year follow-up study in primary progressive multiple sclerosis. J Neurol Neurosurg Psychiatry 82:72-77
10. Bozzali M, Cercignani M, Sormani MP, Comi G, Filippi M (2002) Quantification of brain gray matter damage in different MS phenotypes by use of diffusion tensor MR imaging. AJNR Am J Neuroradiol 23:985-988 (Pubitemid 34663445)
11. Bradl M, Lassmann H (2009) Progressive multiple sclerosis. Semin Immunopathol 31:455-465
12. Bramow S, Frischer JM, Lassmann H, Koch-Henriksen N, Lucchinetti CF, Sorensen PS, Laursen H (2010) Demyelination versus remyelination in progressive multiple sclerosis. Brain 133: 2983-2998
13. Calabrese M, Rocca MA, Atzori M, Mattisi I, Bernardi V, Favaretto A, Barachino L, Romualdi C, Rinaldi L, Perini P, Gallo P, Filippi M (2009) Cortical lesions in primary progressive multiple sclerosis: a 2-year longitudinal MR study. Neurology 72:1330-1336
14. Calabrese M, Battaglini M, Giorgio A, Atzori M, Bernardi V, Mattisi I, Gallo P, De Stefano N (2010) Imaging distribution and frequency of cortical lesions in patients with multiple sclerosis. Neurology 75:1234-1240
15. Ceccarelli A, Rocca MA, Valsasina P, Rodegher M, Pagani E, Falini A, Comi G, Filippi M (2009) A multiparametric evaluation of regional brain damage in patients with primary progressive multiple sclerosis. Hum Brain Mapp 30:3009-3019
16. Ceccarelli A, Rocca MA, Valsasina P, Rodegher M, Falini A, Comi G, Filippi M (2010) Structural and functional magnetic resonance imaging correlates of motor network dysfunction in primary progressive multiple sclerosis. Eur J Neurosci 31: 1273-1280
17. Cercignani M, Bozzali M, Iannucci G, Comi G, Filippi M (2001) Magnetisation transfer ratio and mean diffusivity of normal appearing white and grey matter from patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 70:311-317 (Pubitemid 32250886)
18. Cercignani M, Inglese M, Pagani E, Comi G, Filippi M (2001) Mean diffusivity and fractional anisotropy histograms of patients with multiple sclerosis. AJNR Am J Neuroradiol 22:952-958 (Pubitemid 32436241)
19. Cercignani M, Bozzali M, Iannucci G, Comi G, Filippi M (2002) Intra-voxel and inter-voxel coherence in patients with multiple sclerosis assessed using diffusion tensor MRI. J Neurol 249: 875-883 (Pubitemid 34754225)
20. Ciccarelli O, Werring DJ, Wheeler-Kingshott CA, Barker GJ, Parker GJ, Thompson AJ, Miller DH (2001) Investigation of MS normal-appearing brain using diffusion tensor MRI with clinical correlations. Neurology 56:926-933 (Pubitemid 32290810)
21. Ciccarelli O, Toosy AT, Marsden JF, Wheeler-Kingshott CM, Miller DH, Matthews PM, Thompson AJ (2006) Functional response to active and passive ankle movements with clinical correlations in patients with primary progressive multiple sclerosis. J Neurol 253:882-891 (Pubitemid 44100441)
22. Cottrell DA, Kremenchutzky M, Rice GP, Koopman WJ, Hader W, Baskerville J, Ebers GC (1999) The natural history of multiple sclerosis: a geographically based study. 5. The clinical features and natural history of primary progressive multiple sclerosis. Brain 122(Pt 4):625-639 (Pubitemid 29158771)
23. Cucurella MG, Rovira A, Rio J, Pedraza S, Tintore MM, Montalban X, Alonso J (2000) Proton magnetic resonance spectroscopy in primary and secondary progressive multiple sclerosis. NMR Biomed 13:57-63 (Pubitemid 30230802)
24. Davie CA, Barker GJ, Thompson AJ, Tofts PS, McDonald WI, Miller DH (1997) 1H magnetic resonance spectroscopy of chronic cerebral white matter lesions and normal appearing white matter in multiple sclerosis. J Neurol Neurosurg Psychiatry 63:736-742 (Pubitemid 27520749)
25. Dehmeshki J, Chard DT, Leary SM, Watt HC, Silver NC, Tofts PS, Thompson AJ, Miller DH (2003) The normal appearing grey matter in primary progressive multiple sclerosis: a magnetisation transfer imaging study. J Neurol 250:67-74 (Pubitemid 36206687)
26. Di Perri C, Battaglini M, Stromillo ML, Bartolozzi ML, Guidi L, Federico A, De Stefano N (2008) Voxel-based assessment of differences in damage and distribution of white matter lesions between patients with primary progressive and relapsing-remitting multiple sclerosis. Arch Neurol 65:236-243 (Pubitemid 351240787)
27. Droogan AG, Clark CA, Werring DJ, Barker GJ, McDonald WI, Miller DH (1999) Comparison of multiple sclerosis clinical subgroups using navigated spin echo diffusion-weighted imaging. Magn Reson Imaging 17:653-661 (Pubitemid 29247380)
28. Evangelou N, DeLuca GC, Owens T, Esiri MM (2005) Pathological study of spinal cord atrophy in multiple sclerosis suggests limited role of local lesions. Brain 128:29-34 (Pubitemid 40070517)
29. Filippi M, Rocca MA (2009) Functional MR imaging in multiple sclerosis. Neuroimaging Clin N Am 19:59-70
30. Filippi M, Iannucci G, Tortorella C, Minicucci L, Horsfield MA, Colombo B, Sormani MP, Comi G (1999) Comparison of MS clinical phenotypes using conventional and magnetization transfer MRI. Neurology 52:588-594 (Pubitemid 29075609)
31. Filippi M, Cercignani M, Inglese M, Horsfield MA, Comi G (2001) Diffusion tensor magnetic resonance imaging in multiple sclerosis. Neurology 56:304-311 (Pubitemid 32144139)
32. Filippi M, Rocca MA, Falini A, Caputo D, Ghezzi A, Colombo B, Scotti G, Comi G (2002) Correlations between structural CNS damage and functional MRI changes in primary progressive MS. Neuroimage 15:537-546 (Pubitemid 34852521)
33. Gass A, Barker GJ, Kidd D, Thorpe JW, MacManus D, Brennan A, Tofts PS, Thompson AJ, McDonald WI, Miller DH (1994) Correlation of magnetization transfer ratio with clinical disability in multiple sclerosis. Ann Neurol 36:62-67 (Pubitemid 24205825)
34. Ingle GT, Sastre-Garriga J, Miller DH, Thompson AJ (2005) Is inflammation important in early PPMS? A longitudinal MRI study. J Neurol Neurosurg Psychiatry 76:1255-1258 (Pubitemid 41208379)
35. Khaleeli Z, Cercignani M, Audoin B, Ciccarelli O, Miller DH, Thompson AJ (2007) Localized grey matter damage in early primary progressive multiple sclerosis contributes to disability. Neuroimage 37:253-261 (Pubitemid 47068988)
36. Khaleeli Z, Sastre-Garriga J, Ciccarelli O, Miller DH, Thompson AJ (2007) Magnetisation transfer ratio in the normal appearing white matter predicts progression of disability over 1 year in early primary progressive multiple sclerosis. J Neurol Neurosurg Psychiatry 78:1076-1082
37. Khaleeli Z, Altmann DR, Cercignani M, Ciccarelli O, Miller DH, Thompson AJ (2008) Magnetization transfer ratio in gray matter: a potential surrogate marker for progression in early primary progressive multiple sclerosis. Arch Neurol 65:1454-1459
38. Khaleeli Z, Ciccarelli O, Manfredonia F, Barkhof F, Brochet B, Cercignani M, Dousset V, Filippi M, Montalban X, Polman C, Rovaris M, Rovira A, Sastre-Garriga J, Vellinga M, Miller D, Thompson A (2008) Predicting progression in primary progressive multiple sclerosis: a 10-year multicenter study. Ann Neurol 63:790-793 (Pubitemid 351945538)
39. Khaleeli Z, Ciccarelli O, Mizskiel K, Altmann D, Miller DH, Thompson AJ (2010) Lesion enhancement diminishes with time in primary progressive multiple sclerosis. Mult Scler 16:317-324
40. Kidd D, Thorpe JW, Thompson AJ, Kendall BE, Moseley IF, MacManus DG, McDonald WI, Miller DH (1993) Spinal cord MRI using multi-array coils and fast spin echo. II. Findings in multiple sclerosis. Neurology 43:2632-2637 (Pubitemid 24004558)
41. Kutzelnigg A, Lucchinetti CF, Stadelmann C, Bruck W, Rauschka H, Bergmann M, Schmidbauer M, Parisi JE, Lassmann H (2005) Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 128:2705-2712 (Pubitemid 41552953)
42. Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401-407 (Pubitemid 17173295)
43. Leary SM, Davie CA, Parker GJ, Stevenson VL, Wang L, Barker GJ, Miller DH, Thompson AJ (1999) 1H magnetic resonance spectroscopy of normal appearing white matter in primary progressive multiple sclerosis. J Neurol 246:1023-1026
44. Leary SM, Silver NC, Stevenson VL, Barker GJ, Miller DH, Thompson AJ (1999) Magnetisation transfer of normal appearing white matter in primary progressive multiple sclerosis. Mult Scler 5:313-316 (Pubitemid 29505044)
45. Lycklama a Nijeholt GJ, Castelijns JA, Lazeron RH, van Waesberghe JH, Polman CH, Uitdehaag BM, Barkhof F (2000) Magnetization transfer ratio of the spinal cord in multiple sclerosis: relationship to atrophy and neurologic disability. J Neuroimaging 10:67-72 (Pubitemid 30225298)
46. Lycklama G, Thompson A, Filippi M, Miller D, Polman C, Fazekas F, Barkhof F (2003) Spinal-cord MRI in multiple sclerosis. Lancet Neurol 2:555-562 (Pubitemid 36994995)
47. Mesaros S, Rocca MA, Pagani E, Sormani MP, Petrolini M, Comi G, Filippi M (2011) Thalamic damage predicts the evolution of primary-progressive multiple sclerosis at 5 years. AJNR Am J Neuroradiol 32(6):1016-1020
48. Miller DH, Leary SM (2007) Primary-progressive multiple sclerosis. Lancet Neurol 6:903-912 (Pubitemid 47405002)
49. Mostert JP, Koch MW, Steen C, Heersema DJ, De Groot JC, De Keyser J (2010) T2 lesions and rate of progression of disability in multiple sclerosis. Eur J Neurol 17:1471-1475
50. Mottershead JP, Schmierer K, Clemence M, Thornton JS, Scaravilli F, Barker GJ, Tofts PS, Newcombe J, Cuzner ML, Ordidge RJ, McDonald WI, Miller DH (2003) High field MRI correlates of myelin content and axonal density in multiple sclerosis -a post-mortem study of the spinal cord. J Neurol 250:1293-1301 (Pubitemid 37456888)
51. Narayana PA, Wolinsky JS, Rao SB, He R, Mehta M (2004) Multicentre proton magnetic resonance spectroscopy imaging of primary progressive multiple sclerosis. Mult Scler 10(Suppl 1):S73-S78 (Pubitemid 38807481)
52. Ogawa S, Menon RS, Tank DW, Kim SG, Merkle H, Ellermann JM, Ugurbil K (1993) Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. Biophys J 64:803-812 (Pubitemid 23130347)
53. Penny S, Khaleeli Z, Cipolotti L, Thompson A, Ron M (2010) Early imaging predicts later cognitive impairment in primary progressive multiple sclerosis. Neurology 74:545-552
54. Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893-906 (Pubitemid 26396817)
55. Pike GB, de Stefano N, Narayanan S, Francis GS, Antel JP, Arnold DL (1999) Combined magnetization transfer and proton spectroscopic imaging in the assessment of pathologic brainlesions in multiple sclerosis. AJNR Am J Neuroradiol 20:829-837 (Pubitemid 29536258)
56. Ramio-Torrenta L, Sastre-Garriga J, Ingle GT, Davies GR, Ameen V, Miller DH, Thompson AJ (2006) Abnormalities in normal appearing tissues in early primary progressive multiple sclerosis and their relation to disability: a tissue specific magnetisation transfer study. J Neurol Neurosurg Psychiatry 77:40-45 (Pubitemid 43022688)
57. Riccitelli G, Rocca MA, Pagani E, Rodegher ME, Rossi P, Falini A, Comi G, Filippi M (2010) Cognitive impairment in multiple sclerosis is associated to different patterns of gray matter atrophy according to clinical phenotype. Hum Brain Mapp. doi:10.1002/hbm.21125
58. Rocca MA, Matthews PM, Caputo D, Ghezzi A, Falini A, Scotti G, Comi G, Filippi M (2002) Evidence for widespread movement-associated functional MRI changes in patients with PPMS. Neurology 58:866-872 (Pubitemid 34242060)
59. Rocca MA, Riccitelli G, Rodegher M, Ceccarelli A, Falini A, Falautano M, Meani A, Comi G, Filippi M (2010) Functional MR Imaging correlates of neuropsychological impairment in primaryprogressive multiple sclerosis. AJNR Am J Neuroradiol 31:1240-1246
60. Rocca MA, Valsasina P, Absinta M, Riccitelli G, Rodegher ME, Misci P, Rossi P, Falini A, Comi G, Filippi M (2010) Defaultmode network dysfunction and cognitive impairment in progressive MS. Neurology 74:1252-1259
61. Rovaris M, Bozzali M, Santuccio G, Ghezzi A, Caputo D, Montanari E, Bertolotto A, Bergamaschi R, Capra R, Mancardi G, Martinelli V, Comi G, Filippi M (2001) In vivo assessment of the brain and cervical cord pathology of patients with primary progressive multiple sclerosis. Brain 124:2540-2549 (Pubitemid 33134941)
62. Rovaris M, Bozzali M, Iannucci G, Ghezzi A, Caputo D, Montanari E, Bertolotto A, Bergamaschi R, Capra R, Mancardi GL, Martinelli V, Comi G, Filippi M (2002) Assessment of normal-appearing white and gray matter in patients with primary progressive multiple sclerosis: a diffusion-tensor magnetic resonance imaging study. Arch Neurol 59:1406-1412 (Pubitemid 35014804)
63. Rovaris M, Gallo A, Falini A, Benedetti B, Rossi P, Comola M, Scotti G, Comi G, Filippi M (2005) Axonal injury and overall tissue loss are not related in primary progressive multiple sclerosis. Arch Neurol 62:898-902 (Pubitemid 40973451)
64. Rovaris M, Gallo A, Valsasina P, Benedetti B, Caputo D, Ghezzi A, Montanari E, Sormani MP, Bertolotto A, Mancardi G, Bergamaschi R, Martinelli V, Comi G, Filippi M (2005) Short-term accrual of gray matter pathology in patients with progressive multiple sclerosis: an in vivo study using diffusion tensor MRI. Neuroimage 24:1139-1146 (Pubitemid 40164515)
65. Rovaris M, Gass A, Bammer R, Hickman SJ, Ciccarelli O, Miller DH, Filippi M (2005) Diffusion MRI in multiple sclerosis. Neurology 65:1526-1532 (Pubitemid 41689463)
66. Rovaris M, Judica E, Gallo A, Benedetti B, Sormani MP, Caputo D, Ghezzi A, Montanari E, Bertolotto A, Mancardi G, Bergamaschi R, Martinelli V, Comi G, Filippi M (2006) Grey matter damage predicts the evolution of primary progressive multiple sclerosis at 5 years. Brain 129:2628-2634 (Pubitemid 44522096)
67. Rovaris M, Judica E, Sastre-Garriga J, Rovira A, Sormani MP, Benedetti B, Korteweg T, De Stefano N, Khaleeli Z, Montalban X, Barkhof F, Miller DH, Polman C, Thompson AJ, Filippi M (2008) Large-scale, multicentre, quantitative MRI study of brain and cord damage in primary progressive multiple sclerosis. Mult Scler 14:455-464 (Pubitemid 351943857)
68. Sajja BR, Narayana PA, Wolinsky JS, Ahn CW (2008) Longitudinal magnetic resonance spectroscopic imaging of primary progressive multiple sclerosis patients treated with glatiramer acetate: multicenter study. Mult Scler 14:73-80 (Pubitemid 351541399)
69. Sajja BR, Wolinsky JS, Narayana PA (2009) Proton magnetic resonance spectroscopy in multiple sclerosis. Neuroimaging Clin N Am 19:45-58
70. Sastre-Garriga J, Ingle GT, Chard DT, Cercignani M, Ramio-Torrenta L, Miller DH, Thompson AJ (2005) Grey and white matter volume changes in early primary progressive multiple sclerosis: a longitudinal study. Brain 128:1454-1460 (Pubitemid 40826197)
71. Sastre-Garriga J, Ingle GT, Chard DT, Ramio-Torrenta L, McLean MA, Miller DH, Thompson AJ (2005) Metabolite changes in normal-appearing gray and white matter are linked with disability in early primary progressive multiple sclerosis. Arch Neurol 62:569-573 (Pubitemid 40489887)
72. Sepulcre J, Sastre-Garriga J, Cercignani M, Ingle GT, Miller DH, Thompson AJ (2006) Regional gray matter atrophy in early primary progressive multiple sclerosis: a voxel-based morphometry study. Arch Neurol 63:1175-1180 (Pubitemid 44232328)
73. Suhy J, Rooney WD, Goodkin DE, Capizzano AA, Soher BJ, Maudsley AA, Waubant E, Andersson PB, Weiner MW (2000) 1H MRSI comparison of white matter and lesions in primary progressive and relapsing-remitting MS. Mult Scler 6:148-155 (Pubitemid 30392111)
74. Thompson AJ, Montalban X, Barkhof F, Brochet B, Filippi M, Miller DH, Polman CH, Stevenson VL, McDonald WI (2000) Diagnostic criteria for primary progressive multiple sclerosis: a position paper. Ann Neurol 47:831-835 (Pubitemid 30390209)
75. Tortorella C, Viti B, Bozzali M, Sormani MP, Rizzo G, Gilardi MF, Comi G, Filippi M (2000) A magnetization transfer histogram study of normal-appearing brain tissue in MS. Neurology 54:186-193 (Pubitemid 30038758)
76. Tur C, Khaleeli Z, Ciccarelli O, Altmann DR, Cercignani M, Miller DH, Thompson AJ (2011) Complementary roles of grey matter MTR and T2 lesions in predicting progression in early PPMS. J Neurol Neurosurg Psychiatry 82:423-428
77. Valsasina P, Rocca MA, Absinta M, Agosta F, Caputo D, Comi G, Filippi M (2011) Cervical cord fMRI abnormalities differ between the progressive forms of multiple sclerosis. Hum Brain Mapp (in press)
78. van Waesberghe JH, Kamphorst W, De Groot CJ, van Walderveen MA, Castelijns JA, Ravid R, Lycklama a Nijeholt GJ, van der Valk P, Polman CH, Thompson AJ, Barkhof F (1999) Axonal loss in multiple sclerosis lesions: magnetic resonance imaging insights into substrates of disability. Ann Neurol 46:747-754 (Pubitemid 29518136)
79. Vrenken H, Barkhof F, Uitdehaag BM, Castelijns JA, Polman CH, Pouwels PJ (2005) MR spectroscopic evidence for glial increase but not for neuro-axonal damage in MS normalappearing white matter. Magn Reson Med 53:256-266 (Pubitemid 40171039)