Advances in the application of MRI to amyotrophic lateral sclerosis

Expert Opinion on Medical Diagnostics

Volumn 4, Issue 6, 2010, Pages 483-496

  Turner, Martin R ^a   Modo, Michel ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

biomarker; motor neuron disease; neurodegeneration; neuroimaging

Indexed keywords

AMYOTROPHIC LATERAL SCLEROSIS; AUTOPSY; BRAIN ATROPHY; COGNITIVE DEFECT; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; ELECTROMYOGRAPHY; FRONTAL LOBE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LONGITUDINAL STUDY; MOLECULAR IMAGING; MOTONEURON; MOTOR CORTEX; NUCLEAR MAGNETIC RESONANCE IMAGING; PATIENT MONITORING; POSITRON EMISSION TOMOGRAPHY; PROGNOSIS; PROGRESSIVE MUSCULAR ATROPHY; PYRAMIDAL TRACT; RESPIRATORY FAILURE; REVIEW; SPINAL CORD; TEMPORAL LOBE; THREE DIMENSIONAL IMAGING; TRACTOGRAPHY; TRANSCRANIAL MAGNETIC STIMULATION; VOXEL BASED MORPHOMETRY; WEAKNESS;

EID: 78649239995     PISSN: 17530059     EISSN: 17530067     Source Type: Journal    
DOI: 10.1517/17530059.2010.536836     Document Type: Review

References (108)

1. Kiernan MC, Vucic S, Cheali B, et al. Amyotrophic lateral sclerosis. Lancet 2010; In press
2. Schymick JC, Talbot K, Traynor BJ. Genetics of sporadic amyotrophic lateral sclerosis. Hum Mol Genet 2007;l6(Spec No 2):R233-42
3. Phukan J, Pender NP, Hardiman O. Cognitive impairment in amyotrophic lateral sclerosis. Lancet Neurol 2007;6(11):994-1003 (Pubitemid 47562321)
4. Baumer D, Ansorge O, Almeida M, Talbot K. The role of RNA processing in the pathogenesis of motor neuron degeneration. Expert Rev Mol Med 2010;12:e21
5. Rothstein JD. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann Neurol 2009;65(Suppl l):S3-9
6. Turner MR, Al-Chalabi A, Shaw CE, Leigh PN. Riluzole and motor neuron disease. Pract Neurol 2003;3(3):l60-70
7. Turner MR, Swash M, Ebers GC. Lockhart Clarke's contribution to the description of amyotrophic lateral sclerosis. Brain 2010;133(ll):3470-9
8. Mitchell JD, Callagher P, Gardham J, et al. Timelines in the diagnostic evaluation of people with suspected amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND)-a 20-year review: can we do better? Amyotroph Lateral Scler 2010;ll(6):537-4l
9. Turner MR, Scaber J, Goodfellow JA, et al. The diagnostic pathway and prognosis in bulbar-onset amyotrophic lateral sclerosis. J Neurol Sci 2010;294(l-2):81-5
10. Turner MR, Kiernan MC, Leigh PN, Talbot K. Biomarkers in amyotrophic lateral sclerosis. Lancet Neurol 2009;8(1):94-109
11. Chio A, Logroscino G, Hardiman O, et al. Prognostic factors in ALS: a critical review. Amyotroph Lateral Scler 2009;10(5-6):310-23
12. Brooks BR, Miller RG, Swash M, Munsat TL. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 2000;l(5):293-9
13. Wohlfart G. Collateral regeneration in partially denervated muscles. Neurology 1958;8(3):175-80
14. Ince PG, Evans J, Knopp M, et al. Corticospinal tract degeneration in the progressive muscular atrophy variant of ALS. Neurology 2003;60(8):1252-8
15. Gordon PH, Cheng B, Katz IB, et al. The natural history of primary lateral sclerosis. Neurology 2006;66(5):647-53
16. Traynor BJ, Codd MB, Corr B, et al. Clinical features of amyotrophic lateral sclerosis according to the El Escorial and Airlie House diagnostic criteria: a population-based study. Arch Neurol 2000;57(8):1171-6
17. Douglass CP, Kandler RH, Shaw PJ, McDermott CJ. An evaluation of neuro physiological criteria used in the diagnosis of motor neuron disease. J Neurol Neurosurg Psychiatry 2010;81(6):646-9
18. Filippi M, Agosta F, Abrahams S, et al. EFNS guidelines on the use of neuro imaging in the management of motor neuron diseases. Eur J Neurol 2010;17(4):526-e20
19. Iwasaki Y, Kinoshita M, Ikeda K, et al. MRI in patients with amyotrophic lateral sclerosis: correlation with clinical features. Int J Neurosci 1991;59(4):253-8
20. Waragai M. MRI and clinical features in amyotrophic lateral sclerosis. Neuroradiology 1997;39(12):847-51
21. Turner MR. Reversible diffusion MRI abnormalities and transient mutism after liver transplantation. Neurology 2005;64(1):177
22. Bryan WW, Reisch JS, McDonald G, et al. Magnetic resonance imaging of muscle in amyotrophic lateral sclerosis. Neurology 1998;51(1):110-13
23. Langkammer C, Enzinger C, Quasthoff S, et al. Mapping of iron deposition in conjunction with assessment of nerve fiber tract integrity in amyotrophic lateral sclerosis. J Magn Reson Imaging 2010;31(6):1339-45
24. Ravits JM, La Spada AR. ALS motor phenotype heterogeneity, focality, and spread: deconstructing motor neuron degeneration. Neurology 2009;73(10):805-11
25. Eisen A. Amyotrophic lateral sclerosis-Evolutionary and other perspectives. Muscle Nerve 2009;40(2):297-304
26. Smith MC. Nerve fibre degeneration in the brain in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 1960;23:269-82
27. Brownell B, Oppenheimer DR, Hughes JT. The central nervous system in motor neurone disease. J Neurol Neurosurg Psychiatry 1970;33(3):338-57
28. Maekawa S, Al Sarraj S, Kibble M, et al. Cortical selective vulnerability in Motor Neurone disease: a morphometric study. Brain 2004;127:1237-51
29. Neumann M, Sampathu DM, Kwong LK, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006;3l4(5796):130-3
30. Ludolph AC, Langen KJ, Regard M, et al. Frontal lobe function in amyotrophic lateral sclerosis: a neuropsychologic and positron emission tomography study. Acta Neurol Scand 1992;85(2):81-9
31. Kew JJ, Goldstein LH, Leigh PN, et al. The relationship between abnormalities of cognitive function and cerebral activation in amyotrophic lateral sclerosis. A neuropsychological and positron emission tomography study. Brain 1993;ll6(Pt6):1399-423
32. Turner MR, Hammers A, Al Chalabi A, et al. Distinct cerebral lesions in sporadic and 'D90A' SOD1 ALS: studies with [HCjflumazenil PET. Brain 2005;128(6):1323-9
33. Turner MR, Osei-Lah AD, Hammers A, et al. Abnormal cortical excitability in sporadic but not homozygous D90A SOD1 ALS. J Neurol Neurosurg Psychiatry 2005;76(9):1279-85
34. Vucic S, Nicholson GA, Kiernan MC. Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis. Brain 2008;131(Pt6):1540- 50
35. Aggarwal A, Nicholson G. Detection of preclinical motor neurone loss in SOD1 mutation carriers using motor unit number estimation. J Neurol Neurosurg Psychiatry 2002;73(2): 199-201
36. Peretti-Viton P, Azulay JP, Trefouret S, et al. MRI of the intracranial corticospinal tracts in amyotrophic and primary lateral sclerosis. Neuroradiology 1999;4l(10):744-9
37. Filippini N, Douaud G, Mackay CE, et al. Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis. Neurology 2010; In press
38. KassubekJ, Unrath A, Huppertz HJ, et al. Global brain atrophy and corticospinal tract alterations in ALS, as investigated by voxel-based morphometry of 3-D MRI. Amyotroph Lateral Scler Other Motor Neuron Disord 2005;6(4):213-20
39. Grosskreutz J, Kaufmann J, Fradrich J, et al. Widespread sensorimotor and frontal cortical atrophy in Amyotrophic Lateral Sclerosis. BMC Neurol 2006;6:17
40. Mezzapesa DM, Ceccarelli A, Dicuonzo F, et al. Whole-brain and regional brain atrophy in amyotrophic lateral sclerosis. AJNR Am J Neuroradiol 2007;28(2):255-9
41. Agosta F, Pagani E, Rocca MA, et al. Voxel-based morphometry study of brain volumetry and diffusivity in amyotrophic lateral sclerosis patients with mild disability. Hum Brain Mapp 2007;28(12):l430-8
42. Roccatagliata L, Bonzano L, Mancardi G, et al. Detection of motor cortex thinning and corticospinal tract involvement by quantitative MRI in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2008:1-6
43. Chang JL, Lomen-Hoerth C, Murphy J, et al. A voxel-based morphometry study of patterns of brain atrophy in ALS and ALS/FTLD. Neurology 2005;65(l):75-80
44. Tartaglia MC, Laluz V, Rowe A, et al. Brain atrophy in primary lateral sclerosis. Neurology 2009;72(l4):1236-4l
45. Turner MR, Hammers A, Allsop J, et al. Volumetric cortical loss in sporadic and familial amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2007;8(6):343-7
46. Abrahams S, Goldstein LH, Suckling J, et al. Frontotemporal white matter changes in amyotrophic lateral sclerosis. J Neurol 2005;252(3):321-31
47. Abrahams S, Goldstein LH, Al Chalabi A, et al. Relation between cognitive dysfunction and pseudobulbar palsy in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 1997;62(5):464-72
48. Ciccarelli O, Catani M, Johansen-Berg H, et al. Diffusion-based tractography in neurological disorders: concepts, applications, and future developments. Lancet Neurol 2008;7(8):715-27
49. Concha L, Gross DW, Wheatley BM, Beaulieu C. Diffusion tensor imaging of time-dependent axonal and myelin degradation after corpus callosotomy in epilepsy patients. Neuroimage 2006;32(3):1090-9
50. Cosottini M, Giannelli M, Vannozzi F, et al. Evaluation of corticospinal tract impairment in the brain of patients with amyotrophic lateral sclerosis by using diffusion tensor imaging acquisition schemes with different numbers of diffusion-weighting directions. J Comput Assist Tomogr 2010;34(5):746-50
51. Ellis CM, Simmons A, Jones DK, et al. Diffusion tensor MRI assesses corticospinal tract damage in ALS. Neurology 1999;53(5):1051-8
52. Grosskreutz J, Peschel T, Unrath A, et al. Whole brain-based computerized neuroimaging in ALS and other motor neuron disorders. Amyotroph Lateral Scler 2008;9(4):238-48
53. Agosta F, Chio A, Cosottini M, et al. The Present and the Future of Neuroimaging in Amyotrophic Lateral Sclerosis. AJNR Am J Neuroradiol 1 April 2010 [Epub ahead of print]
54. Cosottini M, Giannelli M, Siciliano G, et al. Diffusion-tensor MR imaging of corticospinal tract in amyotrophic lateral sclerosis and progressive muscular atrophy. Radiology 2005;237(l):258-64
55. Wong JC, Concha L, Beaulieu C, et al. Spatial profiling of the corticospinal tract in amyotrophic lateral sclerosis using diffusion tensor imaging. J Neuroimaging 2007;17(3):234-40
56. Sage CA, Peeters RR, Gorner A, et al. Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis. Neuroimage 2007;34(2):486-99
57. Cedarbaum JM, Stambler N, Malta E, et al. The ALSFRS-R a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 1999;169(1-2):13-21
58. Abraham I, Menke R, Filippini N, et al. Baseline corticospinal tract MRI reflects change in disability at six month follow-up [abstract]. Amyotroph Lateral Scler 2010;ll(Suppl. 1):25
59. Ng MC, Ho JT, Ho SL, et al. Abnormal diffusion tensor in nonsymptomatic familial amyotrophic lateral sclerosis with a causative superoxide dismutase 1 mutation. J Magn Reson Imaging 2008;27(1):8-13
60. Sach M, Winkler G, Glauche V, et al. Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain 2004;127(Pt2):340-50
61. Thivard L, Pradat PF, Lehericy S, et al. Diffusion tensor imaging and voxel based morphometry study in amyotrophic lateral sclerosis: relationships with motor disability. J Neurol Neurosurg Psychiatry 2007;78(8):889-92
62. Bartels C, Mertens N, Hofer S, et al. Callosal dysfunction in amyotrophic lateral sclerosis correlates with diffusion tensor imaging of the central motor system. Neuromuscul Disord 2008;18(5):398-407
63. Senda J, Ito M, Watanabe H, et al. Correlation between pyramidal tract degeneration and widespread white matter involvement in amyotrophic lateral sclerosis: a study with tractography and diffusion-tensor imaging. Amyotroph Lateral Scler 2009;10(5-6):288-94
64. Eisen A, Kim S, Pant B. Amyotrophic lateral sclerosis (ALS): a phylogenetic disease of the cortico motoneuron? Muscle Nerve 1992;15(2):219-24
65. Ciccarelli O, Behrens TE, Johansen-Berg H, et al. Investigation of white matter pathology in ALS and PLS using tract-based spatial statistics. Hum Brain Mapp 2009;30(2):6l5-24
66. Riad SM, Hathout H, Huang JC. High T2 signal in primary lateral sclerosis supports the topographic distribution of fibers in the corpus callosum: assessing disease in the primary motor segment. AJNR Am J Neuroradiol 18 March 2010 [Epub ahead of print]
67. Unrath A, Muller HP, Riecker A, et al. Whole brain-based analysis of regional white matter tract alterations in rare motor neuron diseases by diffusion tensor imaging. Hum Brain Mapp 2010;31(ll):1727-40
68. Park HJ, Kim JJ, Lee SK, et al. Corpus callosal connection mapping using cortical gray matter parcellation and DT-MRI. Hum Brain Mapp 2008;29(5):503-l6
69. Abe O, Yamada H, Masutani Y, et al. Amyotrophic lateral sclerosis: diffusion tensor tractography and voxel-based analysis. NMR Biomed 2004;17(6):4ll-6
70. Stanton BR, Shinhmar D, Turner MR, et al. Diffusion tensor imaging in sporadic and familial (D90A SOD1) forms of amyotrophic lateral sclerosis. Arch Neurol 2009;66(1):109-15
71. Sato K, Aoki S, Iwata NK, et al. Diffusion tensor tract-specific analysis of the uncinate fasciculus in patients with amyotrophic lateral sclerosis. Neuroradiology 2010;52(8):729-33
72. Agosta F, Rocca MA, Valsasina P, et al. A longitudinal diffusion tensor MRI study of the cervical cord and brain in ALS patients. J Neurol Neurosurg Psychiatry 2008;80(l):53-5
73. Finsterbusch J. High-resolution diffusion tensor imaging with inner field-of-view EPI. J Magn Reson Imaging 2009;29(4):987-93
74. Valsasina P, Agosta F, Benedetti B, et al. Diffusion anisotropy of the cervical cord is strictly associated with disability in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 2007;78(5):480-4
75. Nair G, Carew JD, Usher S, et al. Diffusion tensor imaging reveals regional differences in the cervical spinal cord in amyotrophic lateral sclerosis. Neuroimage 2010;53(2):576-83
76. Pioro EP, Antel JP, Cashman NR, Arnold DL. Detection of cortical neuron loss in motor neuron disease by proton magnetic resonance spectroscopic imaging in vivo. Neurology 1994;44(10):1933-8
77. Wang S, Poptani H, Woo JH, et al. Amyotrophic lateral sclerosis: diffusion-tensor and chemical shift MR imaging at 3.0 T. Radiology 2006;239(3):831-8
78. Pohl C, Block W, Karitzky J, et al. Proton magnetic resonance spectroscopy of the motor cortex in 70 patients with amyotrophic lateral sclerosis. ArchNeurol 2001;58(5):729-35
79. Suhy J, Miller RG, Rule R, et al. Early detection and longitudinal changes in amyotrophic lateral sclerosis by (1)H MRSI. Neurology 2002;58(5):773-9
80. Kalra S, Cashman NR, Genge A, Arnold DL. Recovery of N-acetylaspartate in corticomotor neurons of patients with ALS after riluzole therapy. Neuroreport 1998;9(8):1757-61
81. Kalra S, Tai P, Genge A, Arnold DL. Rapid improvement in cortical neuronal integrity in amyotrophic lateral sclerosis detected by proton magnetic resonance spectroscopic imaging. J Neurol 2006;253(8):1060-3
82. Sivak S, Bittsansky M, Kurca E, et al. Proton magnetic resonance spectroscopy in patients with early stages of amyotrophic lateral sclerosis. Neuroradiology 6 April 2010 [Epub ahead of print]
83. Mitsumoto H, Ulug AM, Pullman SL, et al. Quantitative objective markers for upper and lower motor neuron dysfunction in ALS. Neurology 2007;68(17):1402-10
84. Rule RR, Suhy J, Schuff N, et al. Reduced NAA in motor and non-motor brain regions in amyotrophic lateral sclerosis: a cross-sectional and longitudinal study. Amyotroph Lateral Scler Other Motor Neuron Disord 2004;5(3):l4l-9
85. Unrath A, Ludolph AC, Kassubek J. Brain metabolites in definite amyotrophic lateral sclerosis. A longitudinal proton magnetic resonance spectroscopy study. J Neurol 2007;254(8): 1099-106
86. Sharma KR, Kent-Braun JA, Majumdar S, et al. Physiology of fatigue in amyotrophic lateral sclerosis. Neurology l995;45(4):733-40
87. Lule D, Ludolph AC, Kassubek J. MRI-based functional neuroimaging in ALS: an update. Amyotroph Lateral Scler 2009;10(5-6):258-68
88. Beckmann CF, DeLuca M, Devlin JT, Smith SM. Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 2005;360(1457):1001-13
89. Damoiseaux JS, Rombouts SA, Barkhof F, et al. Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 2006;103(37):13848-53
90. Wang K, Liang M, Wang L, et al. Altered functional connectivity in early Alzheimer's disease: a resting-state fMRI study. Hum Brain Mapp 2007;28(10):967-78
91. Mohammadi B, Kollewe K, Samii A, et al. Changes of resting state brain networks in amyotrophic lateral sclerosis. Exp Neurol 2009;217(l):l47-53
92. De Groot CJ, Bergers E, Kamphorst W, et al. Post-mortem MRI-guided sampling of multiple sclerosis brain lesions: increased yield of active demyelinating and (p)reactive lesions. Brain 2001;124(Pt 8):l635-45
93. Seewann A, Kooi EJ, Roosendaal SD, et al. Translating pathology in multiple sclerosis: the combination of postmortem imaging, histopathology and clinical findings. Acta Neurol Scand 2009;119(6):349-55
94. Modo M, Hoehn M, Bulte JW. Cellular MR imaging. Mol Imaging 2005;4(3):l43-64
95. Yamato M, Shiba T, Yamada K, et al. Noninvasive assessment of the brain redox status after transient middle cerebral artery occlusion using Overhauser-enhanced magnetic resonance imaging. J Cereb Blood Flow Metab 2009;29(10):l655-64
96. Hyodo F, Cliuang KH, Goloslievsky AG, et al. Brain redox imaging using blood-brain barrier-permeable nitroxide MRI contrast agent. J Cereb Blood Flow Metab 2008;28(6): 1165-74
97. Tu C, Osborne EA, Louie AY. Synthesis and characterization of a redox-and light-sensitive MRI contrast agent. Tetrahedron 2009;65(7):124l-6
98. Liu CH, Ren JQ, Yang J, et al. DNA-based MRI probes for specific detection of chronic exposure to amphetamine in living brains. J Neurosci 2009;29(34):10663-70
99. Liu PK, Mandeville JB, Guangping D, et al. Transcription MRI: a new view of the living brain. Neuroscientist 2008;l4(5):503-20
100. Klunk WE, Engler H, Nordberg A, et al. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann Neurol 2004;55(3):306-19
101. Vernon AC, Ballard C, Modo M. Neuroimaging for Lewy body disease: is the in vivo molecular imaging of alpha-synuclein neuropathology required and feasible? Brain Res Rev 2010; In press
102. Zhong Z, Deane R, Ali Z, et al. ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat Neurosci 2008;ll(4):420-2
103. McAteer MA, Sibson NR, von Zur Muhlen C, et al. In vivo magnetic resonance imaging of acute brain inflammation using microparticles of iron oxide. Nat Med 2007;13(10):1253-8
104. Turner MR, Cagnin A, Turkheimer FE, et al. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [(11)C](R)-PK11195 positron emission tomography study. Neurobiol Dis 2004;15(3):601-9
105. Saleh A, Schroeter M, Jonkmanns C, et al. In vivo MRI of brain inflammation in human ischaemic stroke. Brain 2004; 127(Pt 7): 1670-7
106. Dousset V, Brochet B, Deloire MS, et al. MR imaging of relapsing multiple sclerosis patients using ultra-small-particle iron oxide and compared with gadolinium. AJNR Am J Neuroradiol 2006;27(5):1000-5
107. Biswal BB, Mennes M, Zuo XN, et al. Toward discovery science of human brain function. Proc Natl Acad Sci USA 2010;107(10):4734-9
108. McNab JA, Voets NL, Jenkinson N, et al. Reduced limbic connections may contraindicate subgenual cingulate deep brain stimulation for intractable depression. J Neurosurg 2009;lll(4):780-4