Measurement of structural integrity of the spinal cord in patients with amyotrophic lateral sclerosis using diffusion tensor magnetic resonance imaging

Autoři: Maximilian Patzig aff001;  Katja Bochmann aff001;  Jürgen Lutz aff001;  Robert Stahl aff001;  Clemens Küpper aff003;  Thomas Liebig aff001;  Peter Reilich aff003;  Marianne Dieterich aff003
Působiště autorů: Institut für Diagnostische und Interventionelle Neuroradiologie, Ludwig-Maximilians-Universität München, München, Germany aff001;  Radiologisches Zentrum München Pasing, München, Germany aff002;  Neurologische Klinik und Poliklinik mit Friedrich-Baur-Institut, Ludwig-Maximilians-Universität München, München, Germany aff003;  Cluster for Systems Neurology, SyNergy, München, Germany aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224078



The value of conventional magnetic resonance imaging (MRI) for amyotrophic lateral sclerosis (ALS) is low. Functional and quantitative MRI could be more accurate. We aimed to examine the value of diffusion tensor imaging (DTI) with fractional anisotropy (FA) measurements of the cervical and upper thoracic spinal cord in patients with ALS.

Patients and methods

Fourteen patients with ALS and 15 sex- and age-matched controls were examined with DTI at a 3T MRI scanner. Region-of-interest (ROI) based fractional anisotropy measurements were performed at the levels C2-C4, C5-C7 and Th1-Th3. ROIs were placed at different anatomical locations of the axial cross sections of the spinal cord.


FA was significantly reduced in ALS patients in anterolateral ROIs and the whole cross section at the C2-C4 level and the cross section of the Th1-Th3 level. There was a trend towards a statistically significant FA reduction in the anterolateral ROIs at the C5-C7 level in ALS patients. No significant differences between patients and controls were found in posterior ROIs.


FA was reduced in ROIs representing the motor tracts in ALS patients. DTI with FA measurements is a promising method in this circumstance. However, for DTI to become a valuable and established method in the diagnostic workup of ALS, larger studies and further standardisation are warranted.

Klíčová slova:

Amyotrophic lateral sclerosis – Anisotropy – Diagnostic medicine – Diffusion tensor imaging – Magnetic resonance imaging – Spinal cord – Spine – Motor neurons


1. Braak H, Brettschneider J, Ludolph AC, Lee VM, Trojanowski JQ, Del Tredici K. Amyotrophic lateral sclerosis—a model of corticofugal axonal spread. Nature reviews Neurology. 2013;9(12):708–14. doi: 10.1038/nrneurol.2013.221

2. Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron D. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotrophic lateral sclerosis and other motor neuron disorders: official publication of the World Federation of Neurology, Research Group on Motor Neuron Diseases. 2000;1(5):293–9. 11464847.

3. de Carvalho M, Dengler R, Eisen A, England JD, Kaji R, Kimura J, et al. Electrodiagnostic criteria for diagnosis of ALS. Clinical neurophysiology: official journal of the International Federation of Clinical Neurophysiology. 2008;119(3):497–503. doi: 10.1016/j.clinph.2007.09.143 18164242.

4. Gupta A, Nguyen TB, Chakraborty S, Bourque PR. Accuracy of Conventional MRI in ALS. The Canadian journal of neurological sciences Le journal canadien des sciences neurologiques. 2014;41(1):53–7. doi: 10.1017/s0317167100016267 24384338.

5. Ngai S, Tang YM, Du L, Stuckey S. Hyperintensity of the precentral gyral subcortical white matter and hypointensity of the precentral gyrus on fluid-attenuated inversion recovery: variation with age and implications for the diagnosis of amyotrophic lateral sclerosis. AJNR American journal of neuroradiology. 2007;28(2):250–4. 17296988.

6. Agosta F, Gorno-Tempini ML, Pagani E, Sala S, Caputo D, Perini M, et al. Longitudinal assessment of grey matter contraction in amyotrophic lateral sclerosis: A tensor based morphometry study. Amyotrophic lateral sclerosis: official publication of the World Federation of Neurology Research Group on Motor Neuron Diseases. 2009;10(3):168–74. doi: 10.1080/17482960802603841 19058055.

7. Kwan JY, Meoded A, Danielian LE, Wu T, Floeter MK. Structural imaging differences and longitudinal changes in primary lateral sclerosis and amyotrophic lateral sclerosis. NeuroImage Clinical. 2012;2:151–60. doi: 10.1016/j.nicl.2012.12.003 24179768.

8. 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. Journal of neurology. 2006;253(8):1060–3. doi: 10.1007/s00415-006-0162-7 16609809.

9. Mitsumoto H, Ulug AM, Pullman SL, Gooch CL, Chan S, Tang MX, et al. Quantitative objective markers for upper and lower motor neuron dysfunction in ALS. Neurology. 2007;68(17):1402–10. doi: 10.1212/01.wnl.0000260065.57832.87 17452585.

10. Unrath A, Ludolph AC, Kassubek J. Brain metabolites in definite amyotrophic lateral sclerosis. A longitudinal proton magnetic resonance spectroscopy study. Journal of neurology. 2007;254(8):1099–106. doi: 10.1007/s00415-006-0495-2 17431700.

11. Menke RA, Abraham I, Thiel CS, Filippini N, Knight S, Talbot K, et al. Fractional anisotropy in the posterior limb of the internal capsule and prognosis in amyotrophic lateral sclerosis. Archives of neurology. 2012;69(11):1493–9. doi: 10.1001/archneurol.2012.1122 22910997.

12. Sage CA, Peeters RR, Gorner A, Robberecht W, Sunaert S. Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis. NeuroImage. 2007;34(2):486–99. doi: 10.1016/j.neuroimage.2006.09.025 17097892.

13. 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: a journal of neurology. 2011;134(Pt 4):1211–28. doi: 10.1093/brain/awr016 21362631.

14. The Amyotrophic Lateral Sclerosis Functional Rating Scale. Assessment of activities of daily living in patients with amyotrophic lateral sclerosis. The ALS CNTF treatment study (ACTS) phase I-II Study Group. Archives of neurology. 1996;53(2):141–7. 8639063.

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). Journal of the neurological sciences. 1999;169(1–2):13–21. doi: 10.1016/s0022-510x(99)00210-5 10540002.

16. Ludolph A, Drory V, Hardiman O, Nakano I, Ravits J, Robberecht W, et al. A revision of the El Escorial criteria—2015. Amyotrophic lateral sclerosis & frontotemporal degeneration. 2015;16(5–6):291–2. doi: 10.3109/21678421.2015.1049183

17. Martin AR, Aleksanderek I, Cohen-Adad J, Tarmohamed Z, Tetreault L, Smith N, et al. Translating state-of-the-art spinal cord MRI techniques to clinical use: A systematic review of clinical studies utilizing DTI, MT, MWF, MRS, and fMRI. NeuroImage Clinical. 2016;10:192–238. doi: 10.1016/j.nicl.2015.11.019 26862478.

18. Valsasina P, Agosta F, Benedetti B, Caputo D, Perini M, Salvi F, et al. Diffusion anisotropy of the cervical cord is strictly associated with disability in amyotrophic lateral sclerosis. Journal of neurology, neurosurgery, and psychiatry. 2007;78(5):480–4. doi: 10.1136/jnnp.2006.100032 17030586.

19. Nair G, Carew JD, Usher S, Lu D, Hu XP, Benatar M. Diffusion tensor imaging reveals regional differences in the cervical spinal cord in amyotrophic lateral sclerosis. NeuroImage. 2010;53(2):576–83. doi: 10.1016/j.neuroimage.2010.06.060 20600964.

20. 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. Journal of neurology, neurosurgery, and psychiatry. 2009;80(1):53–5. doi: 10.1136/jnnp.2008.154252 18931009.

21. Budrewicz S, Szewczyk P, Bladowska J, Podemski R, Koziorowska-Gawron E, Ejma M, et al. The possible meaning of fractional anisotropy measurement of the cervical spinal cord in correct diagnosis of amyotrophic lateral sclerosis. Neurological sciences: official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology. 2016;37(3):417–21. doi: 10.1007/s10072-015-2418-4 26590991.

22. Cohen-Adad J, El Mendili MM, Morizot-Koutlidis R, Lehericy S, Meininger V, Blancho S, et al. Involvement of spinal sensory pathway in ALS and specificity of cord atrophy to lower motor neuron degeneration. Amyotrophic lateral sclerosis & frontotemporal degeneration. 2013;14(1):30–8. doi: 10.3109/17482968.2012.701308 22881412.

23. Underwood CK, Kurniawan ND, Butler TJ, Cowin GJ, Wallace RH. Non-invasive diffusion tensor imaging detects white matter degeneration in the spinal cord of a mouse model of amyotrophic lateral sclerosis. NeuroImage. 2011;55(2):455–61. doi: 10.1016/j.neuroimage.2010.12.044 21185943.

Článek vyšel v časopise


2019 Číslo 10