Association between structural and functional corticospinal involvement in amyotrophic lateral sclerosis assessed by diffusion tensor MRI and triple stimulation technique

Muscle and Nerve

Volumn 49, Issue 4, 2014, Pages 551-557

  Grapperon, Aude Marie ^a   Verschueren, Annie ^a   Duclos, Yann ^a   Confort Gouny, Sylviane ^a   Soulier, Elisabeth ^a   Loundou, Anderson D ^a   Guye, Maxime ^a   Cozzone, Patrick J ^a   Pouget, Jean ^a   Ranjeva, Jean Philippe ^a   Attarian, Shahram ^a  

^a TIMONE HOSPITAL   (France)

Author keywords

Amyotrophic lateral sclerosis; Brain MRI; Diffusion tensor imaging; Transcranial magnetic stimulation; Triple stimulation technique

Indexed keywords

RILUZOLE;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIAGNOSTIC PROCEDURE; DIFFUSION TENSOR IMAGING; DISEASE DURATION; FEMALE; HUMAN; IMAGE DISPLAY; MALE; MIDDLE AGED; NEUROLOGIC EXAMINATION; PARAMETERS; PRIORITY JOURNAL; PYRAMIDAL TRACT; TRANSCRANIAL MAGNETIC STIMULATION; TRIPLE STIMULATION TECHNIQUE;

AMYOTROPHIC LATERAL SCLEROSIS; BRAIN MRI; DIFFUSION TENSOR IMAGING; TRANSCRANIAL MAGNETIC STIMULATION; TRIPLE STIMULATION TECHNIQUE;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; MALE; MIDDLE AGED; PYRAMIDAL TRACTS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84896112999     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.23957     Document Type: Article

References (58)

1. 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;1:293-299.
2. de Carvalho M, Dengler R, Eisen A, England JD, Kaji R, Kimura J, et al. Electrodiagnostic criteria for diagnosis of ALS. Clin Neurophysiol 2008;119:497-503.
3. Chen R, Cros D, Curra A, Di Lazzaro V, Lefaucheur JP, Magistris MR, et al. The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol 2008;119:504-532.
4. Attarian S, Azulay JP, Lardillier D, Verschueren A, Pouget J. Transcranial magnetic stimulation in lower motor neuron diseases. Clin Neurophysiol 2005;116:35-42.
5. Attarian S, Verschueren A, Pouget J. Magnetic stimulation including the triple-stimulation technique in amyotrophic lateral sclerosis. Muscle Nerve 2007;36:55-61.
6. de Carvalho M, Turkman A, Swash M. Motor responses evoked by transcranial magnetic stimulation and peripheral nerve stimulation in the ulnar innervation in amyotrophic lateral sclerosis: the effect of upper and lower motor neuron lesion. J Neuro Sci 2003;210:83-90.
7. Eisen A, Shytbel W, Murphy K, Hoirch M. Cortical magnetic stimulation in amyotrophic lateral sclerosis. Muscle Nerve 1990;13:146-151.
8. Schriefer TN, Hess CW, Mills KR, Murray NM. Central motor conduction studies in motor neurone disease using magnetic brain stimulation. Electroencephalogr Clin Neurophysiol 1989;74:431-437.
9. Magistris MR, Rosler KM, Truffert A, Myers JP. Transcranial stimulation excites virtually all motor neurons supplying the target muscle. A demonstration and a method improving the study of motor evoked potentials. Brain 1998;121(Pt 3):437-450.
10. Kleine BU, Schelhaas HJ, van Elswijk G, de Rijk MC, Stegeman DF, Zwarts MJ. Prospective, blind study of the triple stimulation technique in the diagnosis of ALS. Amyotroph Lateral Scler 2010;11:67-75.
11. Komissarow L, Rollnik JD, Bogdanova D, Krampfl K, Khabirov FA, Kossev A, et al. Triple stimulation technique (TST) in amyotrophic lateral sclerosis. Clin Neurophysiol 2004;115:356-360.
12. Rosler KM, Truffert A, Hess CW, Magistris MR. Quantification of upper motor neuron loss in amyotrophic lateral sclerosis. Clin Neurophysiol 2000;111:2208-2218.
13. Filippi M, Agosta F, Abrahams S, Fazekas F, Grosskreutz J, Kalra S, et al. EFNS guidelines on the use of neuroimaging in the management of motor neuron diseases. Eur J Neurol 2010;17:e526-e520.
14. Foerster BR, Dwamena BA, Petrou M, Carlos RC, Callaghan BC, Pomper MG. Diagnostic accuracy using diffusion tensor imaging in the diagnosis of ALS: a meta-analysis. Acad Radiol 2012;19:1075-1086.
15. Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, 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;169:13-21.
16. Ellis CM, Simmons A, Jones DK, Bland J, Dawson JM, Horsfield MA, et al. Diffusion tensor MRI assesses corticospinal tract damage in ALS. Neurology 1999;53:1051-1058.
17. Iwata NK, Kwan JY, Danielian LE, Butman JA, Tovar-Moll F, Bayat E, et al. White matter alterations differ in primary lateral sclerosis and amyotrophic lateral sclerosis. Brain 2011;134:2642-2655.
18. Hallett M. NINDS myotatic reflex scale. Neurology 1993;43:2723.
19. Litvan I, Mangone CA, Werden W, Bueri JA, Estol CJ, Garcea DO, et al. Reliability of the NINDS Myotatic Reflex Scale. Neurology 1996;47:969-972.
20. Turner MR, Modo M. Advances in the application of MRI to amyotrophic lateral sclerosis. Expert Opin Med Diagn 2010;4:483-496.
21. Catani M, Howard RJ, Pajevic S, Jones DK. Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 2002;17:77-94.
22. Klem GH, Luders HO, Jasper HH, Elger C. The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol 1999;52:3-6.
23. Attarian S, Azulay JP, Verschueren A, Pouget J. Magnetic stimulation using a triple-stimulation technique in patients with multifocal neuropathy without conduction block. Muscle Nerve 2005;32:710-714.
24. Magistris MR, Rosler KM, Truffert A, Landis T, Hess CW. A clinical study of motor evoked potentials using a triple stimulation technique. Brain 1999;122(Pt 2):265-279.
25. Humm AM, Z'Graggen WJ, von Hornstein NE, Magistris MR, Rosler KM. Assessment of central motor conduction to intrinsic hand muscles using the triple stimulation technique: normal values and repeatability. Clin Neurophysiol 2004;115:2558-2566.
26. Attarian S, Pouget J, Schmied A. Covariation of corticospinal efficiency and silent period in motoneuron diseases. Muscle Nerve 2006;34:178-188.
27. Claus D, Brunholzl C, Kerling FP, Henschel S. Transcranial magnetic stimulation as a diagnostic and prognostic test in amyotrophic lateral sclerosis. J Neurol Sci 1995;129(Suppl):30-34.
28. Mills KR, Nithi KA. Peripheral and central motor conduction in amyotrophic lateral sclerosis. J Neurol Sci 1998;159:82-87.
29. Pouget J, Trefouret S, Attarian S. Transcranial magnetic stimulation (TMS): compared sensitivity of different motor response parameters in ALS. Amyotroph Lateral Scler Other Motor Neuron Disord 2000;1(Suppl 2):S45-S49.
30. Triggs WJ, Menkes D, Onorato J, Yan RS, Young MS, Newell K, et al. Transcranial magnetic stimulation identifies upper motor neuron involvement in motor neuron disease. Neurology 1999;53:605-611.
31. Iwata NK, Aoki S, Okabe S, Arai N, Terao Y, Kwak S, et al. Evaluation of corticospinal tracts in ALS with diffusion tensor MRI and brainstem stimulation. Neurology 2008;70:528-532.
32. Sach M, Winkler G, Glauche V, Liepert J, Heimbach B, Koch MA, et al. Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain 2004;127:340-350.
33. Vucic S, Winhammar JM, Rowe DB, Kiernan MC. Corticomotoneuronal function in asymptomatic SOD-1 mutation carriers. Clin Neurophysiol 2010;121:1781-1785.
34. Toosy AT, Werring DJ, Orrell RW, Howard RS, King MD, Barker GJ, et al. Diffusion tensor imaging detects corticospinal tract involvement at multiple levels in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 2003;74:1250-1257.
35. Karlsborg M, Rosenbaum S, Wiegell M, Simonsen H, Larsson H, Werdelin L, et al. Corticospinal tract degeneration and possible pathogenesis in ALS evaluated by MR diffusion tensor imaging. Amyotroph Lateral Scler Other Motor Neuron Disord 2004;5:136-140.
36. Cosottini M, Giannelli M, Siciliano G, Lazzarotti G, Michelassi MC, Del Corona A, et al. Diffusion-tensor MR imaging of corticospinal tract in amyotrophic lateral sclerosis and progressive muscular atrophy. Radiology 2005;237:258-264.
37. Wang S, Poptani H, Woo JH, Desiderio LM, Elman LB, McCluskey LF, et al. Amyotrophic lateral sclerosis: diffusion-tensor and chemical shift MR imaging at 3.0 T. Radiology 2006;239:831-838.
38. Blain CR, Williams VC, Johnston C, Stanton BR, Ganesalingam J, Jarosz JM, et al. A longitudinal study of diffusion tensor MRI in ALS. Amyotroph Lateral Scler 2007;8:348-355.
39. Bartels C, Mertens N, Hofer S, Merboldt KD, Dietrich J, Frahm J, et al. Callosal dysfunction in amyotrophic lateral sclerosis correlates with diffusion tensor imaging of the central motor system. Neuromuscul Disord 2008;18:398-407.
40. Nelles M, Block W, Traber F, Wullner U, Schild HH, Urbach H. Combined 3T diffusion tensor tractography and 1H-MR spectroscopy in motor neuron disease. AJNR Am J Neuroradiol 2008;29:1708-1714.
41. Agosta F, Rocca MA, Valsasina P, Sala S, Caputo D, Perini M, et al. A longitudinal diffusion tensor MRI study of the cervical cord and brain in amyotrophic lateral sclerosis patients. J Neurol Neurosurg Psychiatry 2009;80:53-55.
42. Roccatagliata L, Bonzano L, Mancardi G, Canepa C, Caponnetto C. Detection of motor cortex thinning and corticospinal tract involvement by quantitative MRI in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2009;10:47-52.
43. Metwalli NS, Benatar M, Nair G, Usher S, Hu X, Carew JD. Utility of axial and radial diffusivity from diffusion tensor MRI as markers of neurodegeneration in amyotrophic lateral sclerosis. Brain Res 2010;1348:156-164.
44. Agosta F, Pagani E, Petrolini M, Sormani MP, Caputo D, Perini M, et al. MRI predictors of long-term evolution in amyotrophic lateral sclerosis. Eur J Neurosci 2010;32:1490-1496.
45. Canu E, Agosta F, Riva N, Sala S, Prelle A, Caputo D, et al. The topography of brain microstructural damage in amyotrophic lateral sclerosis assessed using diffusion tensor MR imaging. AJNR Am J Neuroradiol 2011;32:1307-1314.
46. Ben Bashat D, Artzi M, Tarrasch R, Nefussy B, Drory VE, Aizenstein O. A potential tool for the diagnosis of ALS based on diffusion tensor imaging. Amyotroph Lateral Scler 2011;12:398-405.
47. Agosta F, Pagani E, Petrolini M, Caputo D, Perini M, Prelle A, et al. Assessment of white matter tract damage in patients with amyotrophic lateral sclerosis: a diffusion tensor MR imaging tractography study. AJNR Am J Neuroradiol 2010;31:1457-1461.
48. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005;26:132-140.
49. Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics 2007;4:316-329.
50. Hughes JT. Pathology of amyotrophic lateral sclerosis. Adv Neurol 1982;36:61-74.
51. Cirillo M, Esposito F, Tedeschi G, Caiazzo G, Sagnelli A, Piccirillo G, et al. Widespread microstructural white matter involvement in amyotrophic lateral sclerosis: a whole-brain DTI study. AJNR Am J Neuroradiol 2012;33:1102-1108.
52. Filippini N, Douaud G, Mackay CE, Knight S, Talbot K, Turner MR. Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis. Neurology 2010;75:1645-1652.
53. Wong JC, Concha L, Beaulieu C, Johnston W, Allen PS, Kalra S. Spatial profiling of the corticospinal tract in amyotrophic lateral sclerosis using diffusion tensor imaging. J Neuroimaging 2007;17:234-240.
54. Prudlo J, Bissbort C, Glass A, Grossmann A, Hauenstein K, Benecke R, et al. White matter pathology in ALS and lower motor neuron ALS variants: a diffusion tensor imaging study using tract-based spatial statistics. J Neurol 2012;259:1848-1859.
55. van der Graaff MM, Sage CA, Caan MW, Akkerman EM, Lavini C, Majoie CB, et al. Upper and extra-motoneuron involvement in early motoneuron disease: a diffusion tensor imaging study. Brain 2011;134:1211-1228.
56. Ince PG, Evans J, Knopp M, Forster G, Hamdalla HH, Wharton SB, et al. Corticospinal tract degeneration in the progressive muscular atrophy variant of ALS. Neurology 2003;60:1252-1258.
57. Rowland LP. Progressive muscular atrophy and other lower motor neuron syndromes of adults. Muscle Nerve 2010;41:161-165.
58. Kim WK, Liu X, Sandner J, Pasmantier M, Andrews J, Rowland LP, et al. Study of 962 patients indicates progressive muscular atrophy is a form of ALS. Neurology 2009;73:1686-1692.