Longitudinal diffusion tensor imaging in amyotrophic lateral sclerosis

BMC Neuroscience

Julian Grosskreutz¹  Reinhard Dengler²  Viktor Hartung¹  Thomas Peschel³  Tino Prell¹  Carsten Keil² 

[1] Department of Neurology, Jena University Hospital, Erlanger Allee 101, Jena, 07747, Germany;Department of Neurology and Clinical Neurophysiology, Medical School Hannover, Carl-Neuberg-Str.1, Hannover, 30625, Germany;Department of Psychiatry and Psychotherapy, Medical School Hannover, Carl-Neuberg-Strasse 1, Hannover, 30625, Germany

关键词: Follow-up;    Diffusion tensor imaging;    Amyotrophic lateral sclerosis;    Cerebellum;   

Others  :  1140792
DOI  :  10.1186/1471-2202-13-141

 received in 2012-05-12, accepted in 2012-10-31,  发布年份 2012

【 摘 要 】

Background

Amyotrophic lateral sclerosis (ALS) is a fatal neurodegenerative disorder, caused by progressive loss of motor neurons. Changes are widespread in the subcortical white matter in ALS. Diffusion tensor imaging (DTI) detects pathological changes in white matter fibres in vivo, based on alterations in the degree (diffusivity, ADC) and directedness (fractional anisotropy, FA) of proton movement.

Methods

24 patients with ALS and 24 age-matched controls received 1.5T DTI. FA and ADC were analyzed using statistical parametric mapping. In 15 of the 24 ALS patients, a second DTI was obtained after 6 months.

Results

Decreased FA in the corticospinal tract (CST) and frontal areas confirm existing results. With a direct comparison of baseline and follow-up dataset, the progression of upper motor neuron degeneration, reflected in FA decrease, could be captured along the CST and in frontal areas. The involvement of cerebellum in the pathology of ALS, as suspected from functional MRI studies, could be confirmed by a reduced FA (culmen, declive). These structural changes correlated well with disease duration, ALSFRS-R, and physical and executive functions.

Conclusion

DTI detects changes that are regarded as prominent features of ALS and thus, shows promise in its function as a biomarker. Using the technique herein, we could demonstrate DTI changes at follow-up which correlated well with clinical progression.

【 授权许可】

   
2012 Keil et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Smith MC: Nerve fibre degeneration in the brain in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 1960, 23:269-282.
• [2]Rafalowska J, Dziewulska D: White matter injury in amyotrophic lateral sclerosis (ALS). Folia Neuropathol 1996, 34:87-91.
• [3]Grosskreutz J, Peschel T, Unrath A, Dengler R, Ludolph AC, Kassubek J: Whole brain-based computerized neuroimaging in ALS and other motor neuron disorders. Amyotroph Lateral Scler 2008, 9:238-248.
• [4]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.
• [5]Abe O, Yamada H, Masutani Y, Aoki S, Kunimatsu A, Yamasue H, et al.: Amyotrophic lateral sclerosis: diffusion tensor tractography and voxel-based analysis. NMR Biomed 2004, 17:411-416.
• [6]Agosta F, Pagani E, Rocca MA, Caputo D, Perini M, Salvi F, et al.: Voxel-based morphometry study of brain volumetry and diffusivity in amyotrophic lateral sclerosis patients with mild disability. Hum Brain Mapp 2007, 28:1430-1438.
• [7]Sage CA, Peeters RR, Gorner A, Robberecht W, Sunaert S: Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis. Neuroimage 2007, 34:486-499.
• [8]Muller HP, Lule D, Unrath A, Ludolph AC, Riecker A, Kassubek J: Complementary image analysis of diffusion tensor imaging and 3-dimensional t1-weighted imaging: white matter analysis in amyotrophic lateral sclerosis. J Neuroimaging 2011, 21:24-33.
• [9]Douaud G, Filippini N, Knight S, Talbot K, Turner MR: Integration of structural and functional magnetic resonance imaging in amyotrophic lateral sclerosis. Brain 2011, 134(Pt 12):3470-3479.
• [10]Grosskreutz J, Kaufmann J, Fradrich J, Dengler R, Heinze HJ, Peschel T: Widespread sensorimotor and frontal cortical atrophy in Amyotrophic Lateral Sclerosis. BMC Neurol 2006, 6:17. BioMed Central Full Text
• [11]Grosskreutz J, Kaufmann J, Fraedrich J, Dengler R, Heinze HJ, Peschel T: Widespread sensorimotor and frontal cortical atrophy in Amyotrophic Lateral Sclerosis. BMC Neurol 2006, 6:17. BioMed Central Full Text
• [12]Turner MR, Cagnin A, Turkheimer FE, Miller CC, Shaw CE, Brooks DJ, et al.: Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study. Neurobiol Dis 2004, 15:601-609.
• [13]Beaulieu C: The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 2002, 15:435-455.
• [14]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.
• [15]Graham JM, Papadakis N, Evans J, Widjaja E, Romanowski CA, Paley MN, et al.: Diffusion tensor imaging for the assessment of upper motor neuron integrity in ALS. Neurology 2004, 63:2111-2119.
• [16]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.
• [17]Yin H, Cheng SHT, Zhang J, Ma L, Gao Y, Li D, et al.: Corticospinal tract degeneration in amyotrophic lateral sclerosis: a diffusion tensor imaging and fibre tractography study. Ann Acad Med Singapore 2008, 37:411-415.
• [18]Lombardo F, Frijia F, Bongioanni P, Canapicchi R, Minichilli F, Bianchi F, et al.: Diffusion tensor MRI and MR spectroscopy in long lasting upper motor neuron involvement in amyotrophic lateral sclerosis. Arch Ital Biol 2009, 147:69-82.
• [19]Sage CA, Van Hecke W, Peeters R, Sijbers J, Robberecht W, Parizel P, et al.: Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis: revisited. Hum Brain Mapp 2009, 30:3657-3675.
• [20]Senda J, Ito M, Watanabe H, Atsuta N, Kawai Y, Katsuno M, 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):288-294.
• [21]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.
• [22]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.
• [23]Li J, Pan P, Song W, Huang R, Chen K, Shang H: A meta-analysis of diffusion tensor imaging studies in amyotrophic lateral sclerosis. Neurobiol.Aging 2011, 33(8):1833-1888.
• [24]Ellis CM, Suckling J, Amaro E Jr, Bullmore ET, Simmons A, Williams SC, et al.: Volumetric analysis reveals corticospinal tract degeneration and extramotor involvement in ALS. Neurology 2001, 57:1571-1578.
• [25]Chang JL, Lomen-Hoerth C, Murphy J, Henry RG, Kramer JH, Miller BL, et al.: A voxel-based morphometry study of patterns of brain atrophy in ALS and ALS/FTLD. Neurology 2005, 65:75-80.
• [26]Kassubek J, Unrath A, Huppertz HJ, Lule D, Ethofer T, Sperfeld AD, 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, 6:213-220.
• [27]Ciccarelli O, Behrens TE, Johansen-Berg H, Talbot K, Orrell RW, Howard RS, et al.: Investigation of white matter pathology in ALS and PLS using tract-based spatial statistics. Hum Brain Mapp 2009, 30:615-624.
• [28]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.
• [29]Abrahams S, Leigh PN, Goldstein LH: Cognitive change in ALS: a prospective study. Neurology 2005, 64:1222-1226.
• [30]Raaphorst J, de Visser M, van Tol MJ, Linssen WH, van der Kooi AJ, de Haan RJ, et al.: Cognitive dysfunction in lower motor neuron disease: executive and memory deficits in progressive muscular atrophy. J Neurol Neurosurg Psychiatry 2011, 82:170-175.
• [31]Swash M, Scholtz CL, Vowles G, Ingram DA: Selective and asymmetric vulnerability of corticospinal and spinocerebellar tracts in motor neuron disease. J Neurol Neurosurg Psychiatry 1988, 51:785-789.
• [32]Takahashi H, Oyanagi K, Ikuta F, Tanaka M, Yuasa T, Miyatake T: Widespread multiple system degeneration in a patient with familial amyotrophic lateral sclerosis. J Neurol Sci 1993, 120:15-21.
• [33]Konrad C, Henningsen H, Bremer J, Mock B, Deppe M, Buchinger C, et al.: Pattern of cortical reorganization in amyotrophic lateral sclerosis: a functional magnetic resonance imaging study. Exp Brain Res 2002, 143:51-56.
• [34]Konrad C, Jansen A, Henningsen H, Sommer J, Turski PA, Brooks BR, et al.: Subcortical reorganization in amyotrophic lateral sclerosis. Exp Brain Res 2006, 172:361-369.
• [35]Schoenfeld MA, Tempelmann C, Gaul C, Kuhnel GR, Duzel E, Hopf JM, et al.: Functional motor compensation in amyotrophic lateral sclerosis. J Neurol 2005, 252:944-952.
• [36]Han J, Ma L: Functional magnetic resonance imaging study of the brain in patients with amyotrophic lateral sclerosis. Chin Med Sci J 2006, 21:228-233.
• [37]Agosta F, Valsasina P, Absinta M, Riva N, Sala S, Prelle A, et al.: Sensorimotor functional connectivity changes in amyotrophic lateral sclerosis. Cereb Cortex 2011, 21:2291-2298.
• [38]Thivard L, Pradat PF, Lehericy S, Lacomblez L, Dormont D, Chiras J, et al.: Diffusion tensor imaging and voxel based morphometry study in amyotrophic lateral sclerosis: relationships with motor disability. J Neurol Neurosurg Psychiatry 2007, 78:889-892.
• [39]Penhune VB, Doyon J: Cerebellum and M1 interaction during early learning of timed motor sequences. Neuroimage 2005, 26:801-812.
• [40]Jacob S, Finsterbusch J, Weishaupt JH, Khorram-Sefat D, Frahm J, Ehrenreich H: Diffusion tensor imaging for long-term follow-up of corticospinal tract degeneration in amyotrophic lateral sclerosis. Neuroradiology 2003, 45:598-600.
• [41]Nickerson JP, Koski CJ, Boyer AC, Burbank HN, Tandan R, Filippi CG: Linear longitudinal decline in fractional anisotropy in patients with amyotrophic lateral sclerosis: preliminary results. Klin Neuroradiol 2009, 19:129-134.
• [42]Zhang Y, Schuff N, Woolley SC, Chiang GC, Boreta L, Laxamana J, et al.: Progression of white matter degeneration in amyotrophic lateral sclerosis: A diffusion tensor imaging study. Amyotroph Lateral Scler 2011, 12:421-429.
• [43]Senda J, Kato S, Kaga T, Ito M, Atsuta N, Nakamura T, et al.: Progressive and widespread brain damage in ALS: MRI voxel-based morphometry and diffusion tensor imaging study. Amyotroph Lateral Scler 2011, 12:59-69.
• [44]Turner MR, Grosskreutz J, Kassubek J, Abrahams S, Agosta F, Benatar M, et al.: Towards a neuroimaging biomarker for amyotrophic lateral sclerosis. Lancet Neurol 2011, 10:400-403.