Skip to main content
Top
Published in: BMC Neurology 1/2016

Open Access 01-12-2016 | Research article

The value of magnetic resonance imaging as a biomarker for amyotrophic lateral sclerosis: a systematic review

Authors: G. Grolez, C. Moreau, V. Danel-Brunaud, C. Delmaire, R. Lopes, P. F. Pradat, M. M. El Mendili, L. Defebvre, D. Devos

Published in: BMC Neurology | Issue 1/2016

Login to get access

Abstract

Background

Amyotrophic lateral sclerosis (ALS) is a fatal, rapidly progressive neurodegenerative disease that mainly affects the motor system. A number of potentially neuroprotective and neurorestorative disease-modifying drugs are currently in clinical development. At present, the evaluation of a drug’s clinical efficacy in ALS is based on the ALS Functional Rating Scale Revised, motor tests and survival. However, these endpoints are general, variable and late-stage measures of the ALS disease process and thus require the long-term assessment of large cohorts. Hence, there is a need for more sensitive radiological biomarkers. Various sequences for magnetic resonance imaging (MRI) of the brain and spinal cord have may have value as surrogate biomarkers for use in future clinical trials. Here, we review the MRI findings in ALS, their clinical correlations, and their limitations and potential role as biomarkers.

Methods

The PubMed database was screened to identify studies using MRI in ALS. We included general MRI studies with a control group and an ALS group and longitudinal studies even if a control group was lacking.

Results

A total of 116 studies were analysed with MRI data and clinical correlations. The most disease-sensitive MRI patterns are in motor regions but the brain is more broadly affected.

Conclusion

Despite the existing MRI biomarkers, there is a need for large cohorts with long term MRI and clinical follow-up. MRI assessment could be improved by standardized MRI protocols with multicentre studies.
Literature
1.
go back to reference Bensimon G, Lacomblez L, Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N Engl J Med. 1994;330(9):585–91.PubMed Bensimon G, Lacomblez L, Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N Engl J Med. 1994;330(9):585–91.PubMed
2.
go back to reference Soriani M-H, Desnuelle C. Épidémiologie de la SLA. Rev Neurol (Paris). 2009;165(8–9):627–40. Soriani M-H, Desnuelle C. Épidémiologie de la SLA. Rev Neurol (Paris). 2009;165(8–9):627–40.
3.
go back to reference Beghi E, Logroscino G, Chiò A, Hardiman O, Mitchell D, Swingler R, et al. The epidemiology of ALS and the role of population-based registries. Biochim Biophys Acta (BBA) - Mol Basis Dis. 2006;1762(11–12):1150–7. Beghi E, Logroscino G, Chiò A, Hardiman O, Mitchell D, Swingler R, et al. The epidemiology of ALS and the role of population-based registries. Biochim Biophys Acta (BBA) - Mol Basis Dis. 2006;1762(11–12):1150–7.
4.
go back to reference Mitchell JD, Borasio GD. Amyotrophic lateral sclerosis. Lancet. 2007;369(9578):2031–41.PubMed Mitchell JD, Borasio GD. Amyotrophic lateral sclerosis. Lancet. 2007;369(9578):2031–41.PubMed
5.
go back to reference Turner MR, Bowser R, Bruijn L, Dupuis L, Ludolph A, Mcgrath M, et al. Mechanisms, models and biomarkers in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Front Degener. 2013;14(S1):19–32. Turner MR, Bowser R, Bruijn L, Dupuis L, Ludolph A, Mcgrath M, et al. Mechanisms, models and biomarkers in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Front Degener. 2013;14(S1):19–32.
6.
go back to reference Devos D, Moreau C, Devedjian JC, Kluza J, Petrault M, Laloux C, et al. Targeting Chelatable Iron as a Therapeutic Modality in Parkinson’s Disease. Antioxid Redox Signal. 2014;21(2):195–210.PubMedPubMedCentral Devos D, Moreau C, Devedjian JC, Kluza J, Petrault M, Laloux C, et al. Targeting Chelatable Iron as a Therapeutic Modality in Parkinson’s Disease. Antioxid Redox Signal. 2014;21(2):195–210.PubMedPubMedCentral
7.
go back to reference Kwan JY, Jeong SY, Van Gelderen P, Deng H-X, Quezado MM, Danielian LE, et al. Iron Accumulation in Deep Cortical Layers Accounts for MRI Signal Abnormalities in ALS: Correlating 7 Tesla MRI and Pathology. Ashizawa T, editor. PLoS ONE. 2012 Apr 17;7(4):e35241. Kwan JY, Jeong SY, Van Gelderen P, Deng H-X, Quezado MM, Danielian LE, et al. Iron Accumulation in Deep Cortical Layers Accounts for MRI Signal Abnormalities in ALS: Correlating 7 Tesla MRI and Pathology. Ashizawa T, editor. PLoS ONE. 2012 Apr 17;7(4):e35241.
8.
go back to reference Jeong SY, Rathore KI, Schulz K, Ponka P, Arosio P, David S. Dysregulation of Iron Homeostasis in the CNS Contributes to Disease Progression in a Mouse Model of Amyotrophic Lateral Sclerosis. J Neurosci. 2009;29(3):610–9.PubMed Jeong SY, Rathore KI, Schulz K, Ponka P, Arosio P, David S. Dysregulation of Iron Homeostasis in the CNS Contributes to Disease Progression in a Mouse Model of Amyotrophic Lateral Sclerosis. J Neurosci. 2009;29(3):610–9.PubMed
9.
go back to reference Kollewe K, Mauss U, Krampfl K, Petri S, Dengler R, Mohammadi B. ALSFRS-R score and its ratio: A useful predictor for ALS-progression. J Neurol Sci. 2008;275(1–2):69–73.PubMed Kollewe K, Mauss U, Krampfl K, Petri S, Dengler R, Mohammadi B. ALSFRS-R score and its ratio: A useful predictor for ALS-progression. J Neurol Sci. 2008;275(1–2):69–73.PubMed
10.
go back to reference Rudnicki SA, Berry JD, Ingersoll E, Archibald D, Cudkowicz ME, Kerr DA, et al. Dexpramipexole effects on functional decline and survival in subjects with amyotrophic lateral sclerosis in a Phase II study: Subgroup analysis of demographic and clinical characteristics. Amyotroph Lateral Scler Front Degener. 2013;14(1):44–51. Rudnicki SA, Berry JD, Ingersoll E, Archibald D, Cudkowicz ME, Kerr DA, et al. Dexpramipexole effects on functional decline and survival in subjects with amyotrophic lateral sclerosis in a Phase II study: Subgroup analysis of demographic and clinical characteristics. Amyotroph Lateral Scler Front Degener. 2013;14(1):44–51.
11.
go back to reference Braak H, Brettschneider J, Ludolph AC, Lee VM, Trojanowski JQ, Tredici KD. Amyotrophic lateral sclerosis—a model of corticofugal axonal spread. Nat Rev Neurol. 2013;9(12):708–14.PubMedPubMedCentral Braak H, Brettschneider J, Ludolph AC, Lee VM, Trojanowski JQ, Tredici KD. Amyotrophic lateral sclerosis—a model of corticofugal axonal spread. Nat Rev Neurol. 2013;9(12):708–14.PubMedPubMedCentral
12.
go back to reference The ALS Schwaben Register Group, Rosenbohm A, Kassubek J, Weydt P, Marroquin N, Volk AE, et al. Can lesions to the motor cortex induce amyotrophic lateral sclerosis? J Neurol. 2014;261(2):283–90. The ALS Schwaben Register Group, Rosenbohm A, Kassubek J, Weydt P, Marroquin N, Volk AE, et al. Can lesions to the motor cortex induce amyotrophic lateral sclerosis? J Neurol. 2014;261(2):283–90.
13.
go back to reference Ravits JM, La Spada AR. ALS motor phenotype heterogeneity, focality, and spread Deconstructing motor neuron degeneration. Neurology. 2009;73(10):805–11.PubMedPubMedCentral Ravits JM, La Spada AR. ALS motor phenotype heterogeneity, focality, and spread Deconstructing motor neuron degeneration. Neurology. 2009;73(10):805–11.PubMedPubMedCentral
14.
go back to reference Stroman PW, Wheeler-Kingshott C, Bacon M, Schwab JM, Bosma R, Brooks J, et al. The current state-of-the-art of spinal cord imaging: Methods. Neuroimage. 2014;84:1070–81.PubMed Stroman PW, Wheeler-Kingshott C, Bacon M, Schwab JM, Bosma R, Brooks J, et al. The current state-of-the-art of spinal cord imaging: Methods. Neuroimage. 2014;84:1070–81.PubMed
15.
go back to reference Verma T, Cohen-Adad J. Effect of respiration on the B 0 field in the human spinal cord at 3T: Effect of Respiration on B 0 Field in Human Spinal Cord. Magn Reson Med. 2014;72(6):1629–36.PubMed Verma T, Cohen-Adad J. Effect of respiration on the B 0 field in the human spinal cord at 3T: Effect of Respiration on B 0 Field in Human Spinal Cord. Magn Reson Med. 2014;72(6):1629–36.PubMed
17.
go back to reference Ashburner J, Friston KJ. Voxel-based morphometry--the methods. Neuroimage. 2000;11(6 Pt 1):805–21.PubMed Ashburner J, Friston KJ. Voxel-based morphometry--the methods. Neuroimage. 2000;11(6 Pt 1):805–21.PubMed
18.
go back to reference Grosskreutz J, Kaufmann J, Frädrich J, Dengler R, Heinze H-J, Peschel T. Widespread sensorimotor and frontal cortical atrophy in amyotrophic lateral sclerosis. BMC Neurol. 2006;6(1):17.PubMedPubMedCentral Grosskreutz J, Kaufmann J, Frädrich J, Dengler R, Heinze H-J, Peschel T. Widespread sensorimotor and frontal cortical atrophy in amyotrophic lateral sclerosis. BMC Neurol. 2006;6(1):17.PubMedPubMedCentral
19.
go back to reference Mezzapesa DM, Ceccarelli A, Dicuonzo F, Carella A, De Caro MF, Lopez M, et al. Whole-brain and regional brain atrophy in amyotrophic lateral sclerosis. AJNR Am J Neuroradiol. 2007;28(2):255–9.PubMed Mezzapesa DM, Ceccarelli A, Dicuonzo F, Carella A, De Caro MF, Lopez M, et al. Whole-brain and regional brain atrophy in amyotrophic lateral sclerosis. AJNR Am J Neuroradiol. 2007;28(2):255–9.PubMed
20.
go back to reference Mezzapesa DM, D’Errico E, Tortelli R, Distaso E, Cortese R, Tursi M, et al. Cortical thinning and clinical heterogeneity in amyotrophic lateral sclerosis. PLoS One. 2013;8(11):e80748.PubMedPubMedCentral Mezzapesa DM, D’Errico E, Tortelli R, Distaso E, Cortese R, Tursi M, et al. Cortical thinning and clinical heterogeneity in amyotrophic lateral sclerosis. PLoS One. 2013;8(11):e80748.PubMedPubMedCentral
21.
go back to reference 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(12):1430–8.PubMed 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(12):1430–8.PubMed
22.
go back to reference 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(1):75–80.PubMed 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(1):75–80.PubMed
23.
go back to reference 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(7):1307–14.PubMed 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(7):1307–14.PubMed
24.
go back to reference Thivard L, Pradat P-F, Lehéricy 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(8):889–92.PubMedPubMedCentral Thivard L, Pradat P-F, Lehéricy 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(8):889–92.PubMedPubMedCentral
25.
go back to reference Schuster C, Kasper E, Machts J, Bittner D, Kaufmann J, Benecke R, et al. Focal thinning of the motor cortex mirrors clinical features of amyotrophic lateral sclerosis and their phenotypes: a neuroimaging study. J Neurol. 2013;260(11):2856–64.PubMed Schuster C, Kasper E, Machts J, Bittner D, Kaufmann J, Benecke R, et al. Focal thinning of the motor cortex mirrors clinical features of amyotrophic lateral sclerosis and their phenotypes: a neuroimaging study. J Neurol. 2013;260(11):2856–64.PubMed
26.
go back to reference Ellis CM, Suckling J, Amaro E, Bullmore ET, Simmons A, Williams SC, et al. Volumetric analysis reveals corticospinal tract degeneration and extramotor involvement in ALS. Neurology. 2001;57(9):1571–8.PubMed Ellis CM, Suckling J, Amaro E, Bullmore ET, Simmons A, Williams SC, et al. Volumetric analysis reveals corticospinal tract degeneration and extramotor involvement in ALS. Neurology. 2001;57(9):1571–8.PubMed
27.
go back to reference Devine MS, Pannek K, Coulthard A, Mccombe PA, Rose SE, Henderson RD. Exposing asymmetric gray matter vulnerability in amyotrophic lateral sclerosis. NeuroImage Clin. 2015;7:782–7.PubMedPubMedCentral Devine MS, Pannek K, Coulthard A, Mccombe PA, Rose SE, Henderson RD. Exposing asymmetric gray matter vulnerability in amyotrophic lateral sclerosis. NeuroImage Clin. 2015;7:782–7.PubMedPubMedCentral
28.
go back to reference Zhang Q, Mao C, Jin J, Niu C, Bai L, Dang J, et al. Side of Limb-Onset Predicts Laterality of Gray Matter Loss in Amyotrophic Lateral Sclerosis. BioMed Res Int. 2014;2014:1–11. Zhang Q, Mao C, Jin J, Niu C, Bai L, Dang J, et al. Side of Limb-Onset Predicts Laterality of Gray Matter Loss in Amyotrophic Lateral Sclerosis. BioMed Res Int. 2014;2014:1–11.
29.
go back to reference Walhout R, Westeneng H-J, Verstraete E, Hendrikse J, Veldink JH, van den Heuvel MP, et al. Cortical thickness in ALS: towards a marker for upper motor neuron involvement. J Neurol Neurosurg Psychiatry. 2015;86(3):288–94.PubMed Walhout R, Westeneng H-J, Verstraete E, Hendrikse J, Veldink JH, van den Heuvel MP, et al. Cortical thickness in ALS: towards a marker for upper motor neuron involvement. J Neurol Neurosurg Psychiatry. 2015;86(3):288–94.PubMed
30.
go back to reference Verstraete E, van den Heuvel MP, Veldink JH, Blanken N, Mandl RC, Hulshoff Pol HE, et al. Motor Network Degeneration in Amyotrophic Lateral Sclerosis: A Structural and Functional Connectivity Study. Zhan W, editor. PLoS ONE. 2010 Oct 27;5(10):e13664. Verstraete E, van den Heuvel MP, Veldink JH, Blanken N, Mandl RC, Hulshoff Pol HE, et al. Motor Network Degeneration in Amyotrophic Lateral Sclerosis: A Structural and Functional Connectivity Study. Zhan W, editor. PLoS ONE. 2010 Oct 27;5(10):e13664.
31.
go back to reference Zhu W, Fu X, Cui F, Yang F, Ren Y, Zhang X, et al. ALFF Value in Right Parahippocampal Gyrus Acts as a Potential Marker Monitoring Amyotrophic Lateral Sclerosis Progression: a Neuropsychological, Voxel-Based Morphometry, and Resting-State Functional MRI Study. J Mol Neurosci [Internet]. 2015 Jun 4 [cited 2015 Jul 29]; Available from: http://link.springer.com/10.1007/s12031-015-0583-9 Zhu W, Fu X, Cui F, Yang F, Ren Y, Zhang X, et al. ALFF Value in Right Parahippocampal Gyrus Acts as a Potential Marker Monitoring Amyotrophic Lateral Sclerosis Progression: a Neuropsychological, Voxel-Based Morphometry, and Resting-State Functional MRI Study. J Mol Neurosci [Internet]. 2015 Jun 4 [cited 2015 Jul 29]; Available from: http://​link.​springer.​com/​10.​1007/​s12031-015-0583-9
32.
go back to reference Kassubek J, Unrath A, Huppertz H, Lulé D, Ethofer T, Sperfeld A, et al. Global brain atrophy and corticospinal tract alterations in ALS, as investigated by voxel‐based morphometry of 3‐D MRI. Amyotroph Lateral Scler. 2005;6(4):213–20. Kassubek J, Unrath A, Huppertz H, Lulé D, Ethofer T, Sperfeld A, et al. Global brain atrophy and corticospinal tract alterations in ALS, as investigated by voxel‐based morphometry of 3‐D MRI. Amyotroph Lateral Scler. 2005;6(4):213–20.
33.
go back to reference 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 J Neurol. 2004;127(Pt 2):340–50. 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 J Neurol. 2004;127(Pt 2):340–50.
34.
go back to reference Sage CA, Peeters RR, Görner A, Robberecht W, Sunaert S. Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis. Neuroimage. 2007;34(2):486–99.PubMed Sage CA, Peeters RR, Görner A, Robberecht W, Sunaert S. Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis. Neuroimage. 2007;34(2):486–99.PubMed
35.
go back to reference Agosta F, Valsasina P, Riva N, Copetti M, Messina MJ, Prelle A, et al. The cortical signature of amyotrophic lateral sclerosis. PLoS One. 2012;7(8):e42816.PubMedPubMedCentral Agosta F, Valsasina P, Riva N, Copetti M, Messina MJ, Prelle A, et al. The cortical signature of amyotrophic lateral sclerosis. PLoS One. 2012;7(8):e42816.PubMedPubMedCentral
36.
go back to reference Cerami C, Dodich A, Canessa N, Crespi C, Iannaccone S, Corbo M, et al. Emotional empathy in amyotrophic lateral sclerosis: a behavioural and voxel-based morphometry study. Amyotroph Lateral Scler Front Degener. 2014;15(1–2):21–9. Cerami C, Dodich A, Canessa N, Crespi C, Iannaccone S, Corbo M, et al. Emotional empathy in amyotrophic lateral sclerosis: a behavioural and voxel-based morphometry study. Amyotroph Lateral Scler Front Degener. 2014;15(1–2):21–9.
37.
go back to reference Bede P, Bokde ALW, Byrne S, Elamin M, McLaughlin RL, Kenna K, et al. Multiparametric MRI study of ALS stratified for the C9orf72 genotype. Neurology. 2013;81(4):361–9.PubMedPubMedCentral Bede P, Bokde ALW, Byrne S, Elamin M, McLaughlin RL, Kenna K, et al. Multiparametric MRI study of ALS stratified for the C9orf72 genotype. Neurology. 2013;81(4):361–9.PubMedPubMedCentral
39.
go back to reference Abdulla S, Machts J, Kaufmann J, Patrick K, Kollewe K, Dengler R, et al. Hippocampal degeneration in patients with amyotrophic lateral sclerosis. Neurobiol Aging. 2014;35(11):2639–45.PubMed Abdulla S, Machts J, Kaufmann J, Patrick K, Kollewe K, Dengler R, et al. Hippocampal degeneration in patients with amyotrophic lateral sclerosis. Neurobiol Aging. 2014;35(11):2639–45.PubMed
40.
go back to reference Chapman MC, Jelsone-Swain L, Fling BW, Johnson TD, Gruis K, Welsh RC. Corpus callosum area in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2012;13(6):589–91.PubMedPubMedCentral Chapman MC, Jelsone-Swain L, Fling BW, Johnson TD, Gruis K, Welsh RC. Corpus callosum area in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2012;13(6):589–91.PubMedPubMedCentral
41.
go back to reference Meadowcroft MD, Mutic NJ, Bigler DC, Wang J, Simmons Z, Connor JR, et al. Histological-MRI correlation in the primary motor cortex of patients with amyotrophic lateral sclerosis: MRI and Histological Analysis of the PMC in ALS. J Magn Reson Imaging. 2015;41(3):665–75.PubMed Meadowcroft MD, Mutic NJ, Bigler DC, Wang J, Simmons Z, Connor JR, et al. Histological-MRI correlation in the primary motor cortex of patients with amyotrophic lateral sclerosis: MRI and Histological Analysis of the PMC in ALS. J Magn Reson Imaging. 2015;41(3):665–75.PubMed
42.
go back to reference Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging JMRI. 2001;13(4):534–46.PubMed Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging JMRI. 2001;13(4):534–46.PubMed
43.
go back to reference Habas C. Basic principles of diffusion tensor MR tractography. J Radiol. 2004;85(3):281–6.PubMed Habas C. Basic principles of diffusion tensor MR tractography. J Radiol. 2004;85(3):281–6.PubMed
44.
go back to reference Yamada K, Sakai K, Akazawa K, Yuen S, Nishimura T. MR tractography: a review of its clinical applications. Magn Reson Med Sci MRMS Off J Jpn Soc Magn Reson Med. 2009;8(4):165–74. Yamada K, Sakai K, Akazawa K, Yuen S, Nishimura T. MR tractography: a review of its clinical applications. Magn Reson Med Sci MRMS Off J Jpn Soc Magn Reson Med. 2009;8(4):165–74.
45.
go back to reference 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(2):615–24.PubMed 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(2):615–24.PubMed
46.
go back to reference 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(2):129–34.PubMed 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(2):129–34.PubMed
47.
go back to reference Stagg CJ, Knight S, Talbot K, Jenkinson M, Maudsley AA, Turner MR. Whole-brain magnetic resonance spectroscopic imaging measures are related to disability in ALS. Neurology. 2013;80(7):610–5.PubMedPubMedCentral Stagg CJ, Knight S, Talbot K, Jenkinson M, Maudsley AA, Turner MR. Whole-brain magnetic resonance spectroscopic imaging measures are related to disability in ALS. Neurology. 2013;80(7):610–5.PubMedPubMedCentral
48.
go back to reference 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(5):411–5.PubMed 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(5):411–5.PubMed
49.
go back to reference 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(7):528–32.PubMed 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(7):528–32.PubMed
50.
go back to reference 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(9):2642–55.PubMedPubMedCentral 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(9):2642–55.PubMedPubMedCentral
51.
go back to reference 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(5):1051–8.PubMed 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(5):1051–8.PubMed
52.
go back to reference 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(11):3657–75.PubMed 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(11):3657–75.PubMed
53.
go back to reference Sarica A, Cerasa A, Vasta R, Perrotta P, Valentino P, Mangone G, et al. Tractography in amyotrophic lateral sclerosis using a novel probabilistic tool: a study with tract-based reconstruction compared to voxel-based approach. J Neurosci Methods. 2014;224:79–87.PubMed Sarica A, Cerasa A, Vasta R, Perrotta P, Valentino P, Mangone G, et al. Tractography in amyotrophic lateral sclerosis using a novel probabilistic tool: a study with tract-based reconstruction compared to voxel-based approach. J Neurosci Methods. 2014;224:79–87.PubMed
54.
go back to reference Schimrigk SK, Bellenberg B, Schlüter M, Stieltjes B, Drescher R, Rexilius J, et al. Diffusion tensor imaging-based fractional anisotropy quantification in the corticospinal tract of patients with amyotrophic lateral sclerosis using a probabilistic mixture model. AJNR Am J Neuroradiol. 2007;28(4):724–30.PubMed Schimrigk SK, Bellenberg B, Schlüter M, Stieltjes B, Drescher R, Rexilius J, et al. Diffusion tensor imaging-based fractional anisotropy quantification in the corticospinal tract of patients with amyotrophic lateral sclerosis using a probabilistic mixture model. AJNR Am J Neuroradiol. 2007;28(4):724–30.PubMed
55.
go back to reference Foerster BR, Carlos RC, Dwamena BA, Callaghan BC, Petrou M, Edden RAE, et al. Multimodal MRI as a diagnostic biomarker for amyotrophic lateral sclerosis. Ann Clin Transl Neurol. 2014;1(2):107–14.PubMedPubMedCentral Foerster BR, Carlos RC, Dwamena BA, Callaghan BC, Petrou M, Edden RAE, et al. Multimodal MRI as a diagnostic biomarker for amyotrophic lateral sclerosis. Ann Clin Transl Neurol. 2014;1(2):107–14.PubMedPubMedCentral
56.
go back to reference 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(18):1645–52.PubMedPubMedCentral 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(18):1645–52.PubMedPubMedCentral
57.
go back to reference Rosskopf J, Müller H-P, Dreyhaupt J, Gorges M, Ludolph AC, Kassubek J. Ex post facto assessment of diffusion tensor imaging metrics from different MRI protocols: Preparing for multicentre studies in ALS. Amyotroph Lateral Scler Front Degener. 2015;9:1–10. Rosskopf J, Müller H-P, Dreyhaupt J, Gorges M, Ludolph AC, Kassubek J. Ex post facto assessment of diffusion tensor imaging metrics from different MRI protocols: Preparing for multicentre studies in ALS. Amyotroph Lateral Scler Front Degener. 2015;9:1–10.
58.
go back to reference Tang M, Chen X, Zhou Q, Liu B, Liu Y, Liu S, et al. Quantitative assessment of amyotrophic lateral sclerosis with diffusion tensor imaging in 3.0 T magnetic resonance. Int J Clin Exp Med. 2015;8(5):8295–303.PubMedPubMedCentral Tang M, Chen X, Zhou Q, Liu B, Liu Y, Liu S, et al. Quantitative assessment of amyotrophic lateral sclerosis with diffusion tensor imaging in 3.0 T magnetic resonance. Int J Clin Exp Med. 2015;8(5):8295–303.PubMedPubMedCentral
59.
go back to reference Pyra T, Hui B, Hanstock C, Concha L, Wong JCT, Beaulieu C, et al. Combined structural and neurochemical evaluation of the corticospinal tract in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2010;11(1–2):157–65.PubMed Pyra T, Hui B, Hanstock C, Concha L, Wong JCT, Beaulieu C, et al. Combined structural and neurochemical evaluation of the corticospinal tract in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2010;11(1–2):157–65.PubMed
60.
go back to reference Prell T, Peschel T, Hartung V, Kaufmann J, Klauschies R, Bodammer N, et al. Diffusion tensor imaging patterns differ in bulbar and limb onset amyotrophic lateral sclerosis. Clin Neurol Neurosurg. 2013;115(8):1281–7.PubMed Prell T, Peschel T, Hartung V, Kaufmann J, Klauschies R, Bodammer N, et al. Diffusion tensor imaging patterns differ in bulbar and limb onset amyotrophic lateral sclerosis. Clin Neurol Neurosurg. 2013;115(8):1281–7.PubMed
61.
go back to reference Keil C, Prell T, Peschel T, Hartung V, Dengler R, Grosskreutz J. Longitudinal diffusion tensor imaging in amyotrophic lateral sclerosis. BMC Neurosci. 2012;13(1):141.PubMedPubMedCentral Keil C, Prell T, Peschel T, Hartung V, Dengler R, Grosskreutz J. Longitudinal diffusion tensor imaging in amyotrophic lateral sclerosis. BMC Neurosci. 2012;13(1):141.PubMedPubMedCentral
62.
go back to reference 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(6):421–9.PubMedPubMedCentral 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(6):421–9.PubMedPubMedCentral
63.
go back to reference Rajagopalan V, Allexandre D, Yue GH, Pioro EP. Diffusion Tensor Imaging Evaluation of Corticospinal Tract Hyperintensity in Upper Motor Neuron-Predominant ALS Patients. J Aging Res. 2011;2011:481745.PubMedPubMedCentral Rajagopalan V, Allexandre D, Yue GH, Pioro EP. Diffusion Tensor Imaging Evaluation of Corticospinal Tract Hyperintensity in Upper Motor Neuron-Predominant ALS Patients. J Aging Res. 2011;2011:481745.PubMedPubMedCentral
64.
go back to reference 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(6):411–6.PubMed 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(6):411–6.PubMed
65.
go back to reference Poujois A, Schneider FC, Faillenot I, Camdessanché J-P, Vandenberghe N, Thomas-Antérion C, et al. Brain plasticity in the motor network is correlated with disease progression in amyotrophic lateral sclerosis: Functional Cerebral Reorganization, Disease Progression, and ALS. Hum Brain Mapp. 2013;34(10):2391–401.PubMed Poujois A, Schneider FC, Faillenot I, Camdessanché J-P, Vandenberghe N, Thomas-Antérion C, et al. Brain plasticity in the motor network is correlated with disease progression in amyotrophic lateral sclerosis: Functional Cerebral Reorganization, Disease Progression, and ALS. Hum Brain Mapp. 2013;34(10):2391–401.PubMed
66.
go back to reference Müller H-P, Lulé 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 Off J Am Soc Neuroimaging. 2011;21(1):24–33. Müller H-P, Lulé 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 Off J Am Soc Neuroimaging. 2011;21(1):24–33.
67.
go back to reference Chapman MC, Jelsone-Swain L, Johnson TD, Gruis KL, Welsh RC. Diffusion tensor MRI of the corpus callosum in amyotrophic lateral sclerosis: DTI of the Corpus Callosum in ALS. J Magn Reson Imaging. 2014;39(3):641–7.PubMed Chapman MC, Jelsone-Swain L, Johnson TD, Gruis KL, Welsh RC. Diffusion tensor MRI of the corpus callosum in amyotrophic lateral sclerosis: DTI of the Corpus Callosum in ALS. J Magn Reson Imaging. 2014;39(3):641–7.PubMed
68.
go back to reference Keller J, Vymazal J, Ridzoň P, Rusina R, Kulišt’ák P, Malíková H, et al. Quantitative brain MR imaging in amyotrophic lateral sclerosis. Magma N Y N. 2011;24(2):67–76. Keller J, Vymazal J, Ridzoň P, Rusina R, Kulišt’ák P, Malíková H, et al. Quantitative brain MR imaging in amyotrophic lateral sclerosis. Magma N Y N. 2011;24(2):67–76.
69.
go back to reference 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;1348:156–64.PubMed 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;1348:156–64.PubMed
70.
go back to reference 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(9):1848–59.PubMed 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(9):1848–59.PubMed
71.
go back to reference Wang S, Poptani H, Bilello M, Wu X, Woo JH, Elman LB, et al. Diffusion tensor imaging in amyotrophic lateral sclerosis: volumetric analysis of the corticospinal tract. Am J Neuroradiol. 2006;27(6):1234–8.PubMed Wang S, Poptani H, Bilello M, Wu X, Woo JH, Elman LB, et al. Diffusion tensor imaging in amyotrophic lateral sclerosis: volumetric analysis of the corticospinal tract. Am J Neuroradiol. 2006;27(6):1234–8.PubMed
72.
go back to reference Brettschneider J, Del Tredici K, Toledo JB, Robinson JL, Irwin DJ, Grossman M, et al. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis: ALS Stages. Ann Neurol. 2013;74(1):20–38.PubMedPubMedCentral Brettschneider J, Del Tredici K, Toledo JB, Robinson JL, Irwin DJ, Grossman M, et al. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis: ALS Stages. Ann Neurol. 2013;74(1):20–38.PubMedPubMedCentral
73.
go back to reference Kassubek J, Muller H-P, Del Tredici K, Brettschneider J, Pinkhardt EH, Lule D, et al. Diffusion tensor imaging analysis of sequential spreading of disease in amyotrophic lateral sclerosis confirms patterns of TDP-43 pathology. Brain. 2014;137(6):1733–40.PubMed Kassubek J, Muller H-P, Del Tredici K, Brettschneider J, Pinkhardt EH, Lule D, et al. Diffusion tensor imaging analysis of sequential spreading of disease in amyotrophic lateral sclerosis confirms patterns of TDP-43 pathology. Brain. 2014;137(6):1733–40.PubMed
74.
go back to reference Ding X-Q, Kollewe K, Blum K, Körner S, Kehbel S, Dengler R, et al. Value of quantitative analysis of routine clinical MRI sequences in ALS. Amyotroph Lateral Scler. 2011;12(6):406–13.PubMed Ding X-Q, Kollewe K, Blum K, Körner S, Kehbel S, Dengler R, et al. Value of quantitative analysis of routine clinical MRI sequences in ALS. Amyotroph Lateral Scler. 2011;12(6):406–13.PubMed
75.
go back to reference Bede P, Elamin M, Byrne S, McLaughlin RL, Kenna K, Vajda A, et al. Patterns of cerebral and cerebellar white matter degeneration in ALS. J Neurol Neurosurg Psychiatry. 2015;86(4):468–70.PubMed Bede P, Elamin M, Byrne S, McLaughlin RL, Kenna K, Vajda A, et al. Patterns of cerebral and cerebellar white matter degeneration in ALS. J Neurol Neurosurg Psychiatry. 2015;86(4):468–70.PubMed
76.
go back to reference 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(9):598–600.PubMed 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(9):598–600.PubMed
77.
go back to reference Menke RAL, 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. Arch Neurol. 2012;69(11):1493.PubMed Menke RAL, 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. Arch Neurol. 2012;69(11):1493.PubMed
78.
go back to reference Menke RAL, Korner S, Filippini N, Douaud G, Knight S, Talbot K, et al. Widespread grey matter pathology dominates the longitudinal cerebral MRI and clinical landscape of amyotrophic lateral sclerosis. Brain. 2014;137(9):2546–55.PubMedPubMedCentral Menke RAL, Korner S, Filippini N, Douaud G, Knight S, Talbot K, et al. Widespread grey matter pathology dominates the longitudinal cerebral MRI and clinical landscape of amyotrophic lateral sclerosis. Brain. 2014;137(9):2546–55.PubMedPubMedCentral
79.
go back to reference 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(3):69–82.PubMed 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(3):69–82.PubMed
80.
go back to reference Cardenas-Blanco A, Machts J, Acosta-Cabronero J, Kaufmann J, Abdulla S, Kollewe K, et al. Central white matter degeneration in bulbar- and limb-onset amyotrophic lateral sclerosis. J Neurol. 2014;261(10):1961–7.PubMed Cardenas-Blanco A, Machts J, Acosta-Cabronero J, Kaufmann J, Abdulla S, Kollewe K, et al. Central white matter degeneration in bulbar- and limb-onset amyotrophic lateral sclerosis. J Neurol. 2014;261(10):1961–7.PubMed
81.
go back to reference Foerster BR, Dwamena BA, Petrou M, Carlos RC, Callaghan BC, Churchill CL, et al. Diagnostic accuracy of diffusion tensor imaging in amyotrophic lateral sclerosis: a systematic review and individual patient data meta-analysis. Acad Radiol. 2013;20(9):1099–106.PubMedPubMedCentral Foerster BR, Dwamena BA, Petrou M, Carlos RC, Callaghan BC, Churchill CL, et al. Diagnostic accuracy of diffusion tensor imaging in amyotrophic lateral sclerosis: a systematic review and individual patient data meta-analysis. Acad Radiol. 2013;20(9):1099–106.PubMedPubMedCentral
82.
go back to reference Galanaud D, Nicoli F, Confort-Gouny S, Le Fur Y, Dormont D, Girard N, et al. Brain magnetic resonance spectroscopy. J Radiol. 2007;88(3 Pt 2):483–96.PubMed Galanaud D, Nicoli F, Confort-Gouny S, Le Fur Y, Dormont D, Girard N, et al. Brain magnetic resonance spectroscopy. J Radiol. 2007;88(3 Pt 2):483–96.PubMed
83.
go back to reference Jissendi Tchofo P, Balériaux D. Brain (1)H-MR spectroscopy in clinical neuroimaging at 3T. J Neuroradiol. 2009;36(1):24–40.PubMed Jissendi Tchofo P, Balériaux D. Brain (1)H-MR spectroscopy in clinical neuroimaging at 3T. J Neuroradiol. 2009;36(1):24–40.PubMed
84.
go back to reference Soares DP, Law M. Magnetic resonance spectroscopy of the brain: review of metabolites and clinical applications. Clin Radiol. 2009;64(1):12–21.PubMed Soares DP, Law M. Magnetic resonance spectroscopy of the brain: review of metabolites and clinical applications. Clin Radiol. 2009;64(1):12–21.PubMed
85.
go back to reference Han J, Ma L. Study of the features of proton MR spectroscopy ((1)H-MRS) on amyotrophic lateral sclerosis. J Magn Reson Imaging JMRI. 2010;31(2):305–8.PubMed Han J, Ma L. Study of the features of proton MR spectroscopy ((1)H-MRS) on amyotrophic lateral sclerosis. J Magn Reson Imaging JMRI. 2010;31(2):305–8.PubMed
86.
go back to reference Rooney WD, Miller RG, Gelinas D, Schuff N, Maudsley AA, Weiner MW. Decreased N-acetylaspartate in motor cortex and corticospinal tract in ALS. Neurology. 1998;50(6):1800–5.PubMed Rooney WD, Miller RG, Gelinas D, Schuff N, Maudsley AA, Weiner MW. Decreased N-acetylaspartate in motor cortex and corticospinal tract in ALS. Neurology. 1998;50(6):1800–5.PubMed
87.
go back to reference Liu C, Jiang R, Yi X, Zhu W, Bu B. Role of diffusion tensor imaging or magnetic resonance spectroscopy in the diagnosis and disability assessment of amyotrophic lateral sclerosis. J Neurol Sci. 2015;348(1–2):206–10.PubMed Liu C, Jiang R, Yi X, Zhu W, Bu B. Role of diffusion tensor imaging or magnetic resonance spectroscopy in the diagnosis and disability assessment of amyotrophic lateral sclerosis. J Neurol Sci. 2015;348(1–2):206–10.PubMed
88.
go back to reference Kalra S, Vitale A, Cashman NR, Genge A, Arnold DL. Cerebral degeneration predicts survival in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2006;77(11):1253–5.PubMedPubMedCentral Kalra S, Vitale A, Cashman NR, Genge A, Arnold DL. Cerebral degeneration predicts survival in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2006;77(11):1253–5.PubMedPubMedCentral
89.
go back to reference Kalra S, Hanstock CC, Martin WW, Allen PS, Johnston WS. Detection of cerebral degeneration in amyotrophic lateral sclerosis using high-field magnetic resonance spectroscopy. Arch Neurol. 2006;63(8):1144–8.PubMed Kalra S, Hanstock CC, Martin WW, Allen PS, Johnston WS. Detection of cerebral degeneration in amyotrophic lateral sclerosis using high-field magnetic resonance spectroscopy. Arch Neurol. 2006;63(8):1144–8.PubMed
90.
go back to reference Cervo A, Cocozza S, Saccà F, Giorgio SMDA, Morra VB, Tedeschi E, et al. The combined use of conventional MRI and MR spectroscopic imaging increases the diagnostic accuracy in amyotrophic lateral sclerosis. Eur J Radiol. 2015;84(1):151–7.PubMed Cervo A, Cocozza S, Saccà F, Giorgio SMDA, Morra VB, Tedeschi E, et al. The combined use of conventional MRI and MR spectroscopic imaging increases the diagnostic accuracy in amyotrophic lateral sclerosis. Eur J Radiol. 2015;84(1):151–7.PubMed
91.
go back to reference Pohl C, Block W, Träber F, Schmidt S, Pels H, Grothe C, et al. Proton magnetic resonance spectroscopy and transcranial magnetic stimulation for the detection of upper motor neuron degeneration in ALS patients. J Neurol Sci. 2001;190(1–2):21–7.PubMed Pohl C, Block W, Träber F, Schmidt S, Pels H, Grothe C, et al. Proton magnetic resonance spectroscopy and transcranial magnetic stimulation for the detection of upper motor neuron degeneration in ALS patients. J Neurol Sci. 2001;190(1–2):21–7.PubMed
92.
go back to reference Govind V, Sharma KR, Maudsley AA, Arheart KL, Saigal G, Sheriff S. Comprehensive evaluation of corticospinal tract metabolites in amyotrophic lateral sclerosis using whole-brain 1H MR spectroscopy. PLoS One. 2012;7(4):e35607.PubMedPubMedCentral Govind V, Sharma KR, Maudsley AA, Arheart KL, Saigal G, Sheriff S. Comprehensive evaluation of corticospinal tract metabolites in amyotrophic lateral sclerosis using whole-brain 1H MR spectroscopy. PLoS One. 2012;7(4):e35607.PubMedPubMedCentral
93.
go back to reference Verma G, Woo JH, Chawla S, Wang S, Sheriff S, Elman LB, et al. Whole-brain analysis of amyotrophic lateral sclerosis by using echo-planar spectroscopic imaging. Radiology. 2013;267(3):851–7.PubMedPubMedCentral Verma G, Woo JH, Chawla S, Wang S, Sheriff S, Elman LB, et al. Whole-brain analysis of amyotrophic lateral sclerosis by using echo-planar spectroscopic imaging. Radiology. 2013;267(3):851–7.PubMedPubMedCentral
94.
go back to reference Bowen BC, Pattany PM, Bradley WG, Murdoch JB, Rotta F, Younis AA, et al. MR imaging and localized proton spectroscopy of the precentral gyrus in amyotrophic lateral sclerosis. Am J Neuroradiol. 2000;21(4):647–58.PubMed Bowen BC, Pattany PM, Bradley WG, Murdoch JB, Rotta F, Younis AA, et al. MR imaging and localized proton spectroscopy of the precentral gyrus in amyotrophic lateral sclerosis. Am J Neuroradiol. 2000;21(4):647–58.PubMed
95.
go back to reference Foerster BR, Callaghan BC, Petrou M, Edden RAE, Chenevert TL, Feldman EL. Decreased motor cortex γ-aminobutyric acid in amyotrophic lateral sclerosis. Neurology. 2012;78(20):1596–600.PubMedPubMedCentral Foerster BR, Callaghan BC, Petrou M, Edden RAE, Chenevert TL, Feldman EL. Decreased motor cortex γ-aminobutyric acid in amyotrophic lateral sclerosis. Neurology. 2012;78(20):1596–600.PubMedPubMedCentral
96.
go back to reference 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.PubMed 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.PubMed
97.
go back to reference Wang Q, Zhang X, Chen S, Zhang X, Zhang S, Youdium M, et al. Prevention of Motor Neuron Degeneration by Novel Iron Chelators in SOD1(G93A) Transgenic Mice of Amyotrophic Lateral Sclerosis. Neurodegener Dis. 2011;8(5):310–21.PubMed Wang Q, Zhang X, Chen S, Zhang X, Zhang S, Youdium M, et al. Prevention of Motor Neuron Degeneration by Novel Iron Chelators in SOD1(G93A) Transgenic Mice of Amyotrophic Lateral Sclerosis. Neurodegener Dis. 2011;8(5):310–21.PubMed
98.
go back to reference Deistung A, Schäfer A, Schweser F, Biedermann U, Turner R, Reichenbach JR. Toward in vivo histology: A comparison of quantitative susceptibility mapping (QSM) with magnitude-, phase-, and R2*-imaging at ultra-high magnetic field strength. Neuroimage. 2013;65:299–314.PubMed Deistung A, Schäfer A, Schweser F, Biedermann U, Turner R, Reichenbach JR. Toward in vivo histology: A comparison of quantitative susceptibility mapping (QSM) with magnitude-, phase-, and R2*-imaging at ultra-high magnetic field strength. Neuroimage. 2013;65:299–314.PubMed
99.
go back to reference Haacke EM, Cheng NYC, House MJ, Liu Q, Neelavalli J, Ogg RJ, et al. Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging. 2005;23(1):1–25.PubMed Haacke EM, Cheng NYC, House MJ, Liu Q, Neelavalli J, Ogg RJ, et al. Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging. 2005;23(1):1–25.PubMed
100.
go back to reference Adachi Y, Sato N, Saito Y, Kimura Y, Nakata Y, Ito K, et al. Usefulness of SWI for the Detection of Iron in the Motor Cortex in Amyotrophic Lateral Sclerosis: Usefulness of SWI for the Diagnoses of ALS. J Neuroimaging. 2015;25(3):443–51.PubMed Adachi Y, Sato N, Saito Y, Kimura Y, Nakata Y, Ito K, et al. Usefulness of SWI for the Detection of Iron in the Motor Cortex in Amyotrophic Lateral Sclerosis: Usefulness of SWI for the Diagnoses of ALS. J Neuroimaging. 2015;25(3):443–51.PubMed
101.
go back to reference Chavhan GB, Babyn PS, Thomas B, Shroff MM, Haacke EM. Principles, Techniques, and Applications of T2*-based MR Imaging and Its Special Applications1. RadioGraphics. 2009;29(5):1433–49.PubMedPubMedCentral Chavhan GB, Babyn PS, Thomas B, Shroff MM, Haacke EM. Principles, Techniques, and Applications of T2*-based MR Imaging and Its Special Applications1. RadioGraphics. 2009;29(5):1433–49.PubMedPubMedCentral
102.
go back to reference Haacke EM, Miao Y, Liu M, Habib CA, Katkuri Y, Liu T, et al. Correlation of putative iron content as represented by changes in R2* and phase with age in deep gray matter of healthy adults. J Magn Reson Imaging JMRI. 2010;32(3):561–76.PubMed Haacke EM, Miao Y, Liu M, Habib CA, Katkuri Y, Liu T, et al. Correlation of putative iron content as represented by changes in R2* and phase with age in deep gray matter of healthy adults. J Magn Reson Imaging JMRI. 2010;32(3):561–76.PubMed
103.
go back to reference Langkammer C, Krebs N, Goessler W, Scheurer E, Ebner F, Yen K, et al. Quantitative MR imaging of brain iron: a postmortem validation study. Radiology. 2010;257(2):455–62.PubMed Langkammer C, Krebs N, Goessler W, Scheurer E, Ebner F, Yen K, et al. Quantitative MR imaging of brain iron: a postmortem validation study. Radiology. 2010;257(2):455–62.PubMed
104.
go back to reference Haacke EM, Liu S, Buch S, Zheng W, Wu D, Ye Y. Quantitative susceptibility mapping: current status and future directions. Magn Reson Imaging. 2015;33(1):1–25.PubMed Haacke EM, Liu S, Buch S, Zheng W, Wu D, Ye Y. Quantitative susceptibility mapping: current status and future directions. Magn Reson Imaging. 2015;33(1):1–25.PubMed
105.
go back to reference Langkammer C, Schweser F, Krebs N, Deistung A, Goessler W, Scheurer E, et al. Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A post mortem validation study. Neuroimage. 2012;62(3):1593–9.PubMedPubMedCentral Langkammer C, Schweser F, Krebs N, Deistung A, Goessler W, Scheurer E, et al. Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A post mortem validation study. Neuroimage. 2012;62(3):1593–9.PubMedPubMedCentral
106.
go back to reference Oba H, Araki T, Ohtomo K, Monzawa S, Uchiyama G, Koizumi K, et al. Amyotrophic lateral sclerosis: T2 shortening in motor cortex at MR imaging. Radiology. 1993;189(3):843–6.PubMed Oba H, Araki T, Ohtomo K, Monzawa S, Uchiyama G, Koizumi K, et al. Amyotrophic lateral sclerosis: T2 shortening in motor cortex at MR imaging. Radiology. 1993;189(3):843–6.PubMed
107.
go back to reference Hecht MJ, Fellner C, Schmid A, Neundörfer B, Fellner FA. Cortical T2 signal shortening in amyotrophic lateral sclerosis is not due to iron deposits. Neuroradiology. 2005;47(11):805–8.PubMed Hecht MJ, Fellner C, Schmid A, Neundörfer B, Fellner FA. Cortical T2 signal shortening in amyotrophic lateral sclerosis is not due to iron deposits. Neuroradiology. 2005;47(11):805–8.PubMed
108.
go back to reference Ignjatović A, Stević Z, Lavrnić S, Daković M, Bačić G. Brain iron MRI: A biomarker for amyotrophic lateral sclerosis: Brain Iron MRI: A Biomarker for ALS. J Magn Reson Imaging. 2013;38(6):1472–9.PubMed Ignjatović A, Stević Z, Lavrnić S, Daković M, Bačić G. Brain iron MRI: A biomarker for amyotrophic lateral sclerosis: Brain Iron MRI: A Biomarker for ALS. J Magn Reson Imaging. 2013;38(6):1472–9.PubMed
109.
go back to reference Yu J, Qi F, Wang N, Gao P, Dai S, Lu Y, et al. Increased iron level in motor cortex of amyotrophic lateral sclerosis patients: An in vivo MR study. Amyotroph Lateral Scler Front Degener. 2014;15(5–6):357–61. Yu J, Qi F, Wang N, Gao P, Dai S, Lu Y, et al. Increased iron level in motor cortex of amyotrophic lateral sclerosis patients: An in vivo MR study. Amyotroph Lateral Scler Front Degener. 2014;15(5–6):357–61.
110.
go back to reference Langkammer C, Enzinger C, Quasthoff S, Grafenauer P, Soellinger M, Fazekas F, et al. Mapping of iron deposition in conjunction with assessment of nerve fiber tract integrity in amyotrophic lateral sclerosis. J Magn Reson Imaging JMRI. 2010;31(6):1339–45.PubMed Langkammer C, Enzinger C, Quasthoff S, Grafenauer P, Soellinger M, Fazekas F, et al. Mapping of iron deposition in conjunction with assessment of nerve fiber tract integrity in amyotrophic lateral sclerosis. J Magn Reson Imaging JMRI. 2010;31(6):1339–45.PubMed
111.
go back to reference Prell T, Hartung V, Tietz F, Penzlin S, Ilse B, Schweser F, et al. Susceptibility-Weighted Imaging Provides Insight into White Matter Damage in Amyotrophic Lateral Sclerosis. Kassubek J, editor. PLOS ONE. 2015 Jun 25;10(6):e0131114. Prell T, Hartung V, Tietz F, Penzlin S, Ilse B, Schweser F, et al. Susceptibility-Weighted Imaging Provides Insight into White Matter Damage in Amyotrophic Lateral Sclerosis. Kassubek J, editor. PLOS ONE. 2015 Jun 25;10(6):e0131114.
112.
go back to reference Schweitzer AD, Liu T, Gupta A, Zheng K, Seedial S, Shtilbans A, et al. Quantitative Susceptibility Mapping of the Motor Cortex in Amyotrophic Lateral Sclerosis and Primary Lateral Sclerosis. Am J Roentgenol. 2015;204(5):1086–92. Schweitzer AD, Liu T, Gupta A, Zheng K, Seedial S, Shtilbans A, et al. Quantitative Susceptibility Mapping of the Motor Cortex in Amyotrophic Lateral Sclerosis and Primary Lateral Sclerosis. Am J Roentgenol. 2015;204(5):1086–92.
113.
go back to reference Branco LMT, De Albuquerque M, De Andrade HMT, Bergo FPG, Nucci A, França MC. Spinal cord atrophy correlates with disease duration and severity in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Front Degener. 2014;15(1–2):93–7. Branco LMT, De Albuquerque M, De Andrade HMT, Bergo FPG, Nucci A, França MC. Spinal cord atrophy correlates with disease duration and severity in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Front Degener. 2014;15(1–2):93–7.
114.
go back to reference Cohen-Adad J, Mendili M-ME, Morizot-Koutlidis R, Lehéricy S, Meininger V, Blancho S, et al. Involvement of spinal sensory pathway in ALS and specificity of cord atrophy to lower motor neuron degeneration. Amyotroph Lateral Scler Front Degener. 2013;14(1):30–8. Cohen-Adad J, Mendili M-ME, Morizot-Koutlidis R, Lehéricy S, Meininger V, Blancho S, et al. Involvement of spinal sensory pathway in ALS and specificity of cord atrophy to lower motor neuron degeneration. Amyotroph Lateral Scler Front Degener. 2013;14(1):30–8.
115.
go back to reference El Mendili M-M, Cohen-Adad J, Pelegrini-Issac M, Rossignol S, Morizot-Koutlidis R, Marchand-Pauvert V, et al. Multi-parametric spinal cord MRI as potential progression marker in amyotrophic lateral sclerosis. PLoS One. 2014;9(4):e95516.PubMedPubMedCentral El Mendili M-M, Cohen-Adad J, Pelegrini-Issac M, Rossignol S, Morizot-Koutlidis R, Marchand-Pauvert V, et al. Multi-parametric spinal cord MRI as potential progression marker in amyotrophic lateral sclerosis. PLoS One. 2014;9(4):e95516.PubMedPubMedCentral
116.
go back to reference Iglesias C, Sangari S, El Mendili M-M, Benali H, Marchand-Pauvert V, Pradat P-F. Electrophysiological and spinal imaging evidences for sensory dysfunction in amyotrophic lateral sclerosis. BMJ Open. 2015;5(2):e007659.PubMedPubMedCentral Iglesias C, Sangari S, El Mendili M-M, Benali H, Marchand-Pauvert V, Pradat P-F. Electrophysiological and spinal imaging evidences for sensory dysfunction in amyotrophic lateral sclerosis. BMJ Open. 2015;5(2):e007659.PubMedPubMedCentral
117.
go back to reference Ikeda K, Murata K, Kawase Y, Kawabe K, Kano O, Yoshii Y, et al. Relationship between cervical cord 1H-magnetic resonance spectroscopy and clinoco-electromyographic profile in amyotrophic lateral sclerosis. Muscle Nerve. 2013;47(1):61–7.PubMed Ikeda K, Murata K, Kawase Y, Kawabe K, Kano O, Yoshii Y, et al. Relationship between cervical cord 1H-magnetic resonance spectroscopy and clinoco-electromyographic profile in amyotrophic lateral sclerosis. Muscle Nerve. 2013;47(1):61–7.PubMed
118.
go back to reference Barkhof F, Haller S, Rombouts SARB. Resting-state functional MR imaging: a new window to the brain. Radiology. 2014;272(1):29–49.PubMed Barkhof F, Haller S, Rombouts SARB. Resting-state functional MR imaging: a new window to the brain. Radiology. 2014;272(1):29–49.PubMed
119.
go back to reference Habas C. Physiological basis of functional MRI. J Radiol. 2002;83(11):1737–41.PubMed Habas C. Physiological basis of functional MRI. J Radiol. 2002;83(11):1737–41.PubMed
120.
go back to reference Delmaire C, Krainik A, Lethuc V, Reyns N, Duffau H, Capelle L, et al. Functional magnetic resonance imaging: physiopathology, techniques and applications. J Radiol. 2007;88(3 Pt 2):497–509.PubMed Delmaire C, Krainik A, Lethuc V, Reyns N, Duffau H, Capelle L, et al. Functional magnetic resonance imaging: physiopathology, techniques and applications. J Radiol. 2007;88(3 Pt 2):497–509.PubMed
121.
123.
go back to reference Agosta F, Canu E, Valsasina P, Riva N, Prelle A, Comi G, et al. Divergent brain network connectivity in amyotrophic lateral sclerosis. Neurobiol Aging. 2013;34(2):419–27.PubMed Agosta F, Canu E, Valsasina P, Riva N, Prelle A, Comi G, et al. Divergent brain network connectivity in amyotrophic lateral sclerosis. Neurobiol Aging. 2013;34(2):419–27.PubMed
125.
go back to reference 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(10):2291–8.PubMed 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(10):2291–8.PubMed
126.
go back to reference Mohammadi B, Kollewe K, Samii A, Krampfl K, Dengler R, Münte TF. Changes of resting state brain networks in amyotrophic lateral sclerosis. Exp Neurol. 2009;217(1):147–53.PubMed Mohammadi B, Kollewe K, Samii A, Krampfl K, Dengler R, Münte TF. Changes of resting state brain networks in amyotrophic lateral sclerosis. Exp Neurol. 2009;217(1):147–53.PubMed
127.
go back to reference 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(12):3470–9.PubMed 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(12):3470–9.PubMed
128.
go back to reference Luo C, Chen Q, Huang R, Chen X, Chen K, Huang X, et al. Patterns of Spontaneous Brain Activity in Amyotrophic Lateral Sclerosis: A Resting-State fMRI Study. Duce JA, editor. PLoS ONE. 2012 Sep 20;7(9):e45470. Luo C, Chen Q, Huang R, Chen X, Chen K, Huang X, et al. Patterns of Spontaneous Brain Activity in Amyotrophic Lateral Sclerosis: A Resting-State fMRI Study. Duce JA, editor. PLoS ONE. 2012 Sep 20;7(9):e45470.
129.
go back to reference Mohammadi B, Kollewe K, Samii A, Dengler R, Münte TF. Functional neuroimaging at different disease stages reveals distinct phases of neuroplastic changes in amyotrophic lateral sclerosis. Hum Brain Mapp. 2011;32(5):750–8.PubMed Mohammadi B, Kollewe K, Samii A, Dengler R, Münte TF. Functional neuroimaging at different disease stages reveals distinct phases of neuroplastic changes in amyotrophic lateral sclerosis. Hum Brain Mapp. 2011;32(5):750–8.PubMed
130.
go back to reference Mohammadi B, Kollewe K, Cole DM, Fellbrich A, Heldmann M, Samii A, et al. Amyotrophic lateral sclerosis affects cortical and subcortical activity underlying motor inhibition and action monitoring: ALS and Motor Inhibition. Hum Brain Mapp. 2015;36(8):2878–89.PubMed Mohammadi B, Kollewe K, Cole DM, Fellbrich A, Heldmann M, Samii A, et al. Amyotrophic lateral sclerosis affects cortical and subcortical activity underlying motor inhibition and action monitoring: ALS and Motor Inhibition. Hum Brain Mapp. 2015;36(8):2878–89.PubMed
131.
go back to reference Kollewe K, Münte TF, Samii A, Dengler R, Petri S, Mohammadi B. Patterns of cortical activity differ in ALS patients with limb and/or bulbar involvement depending on motor tasks. J Neurol. 2011;258(5):804–10.PubMed Kollewe K, Münte TF, Samii A, Dengler R, Petri S, Mohammadi B. Patterns of cortical activity differ in ALS patients with limb and/or bulbar involvement depending on motor tasks. J Neurol. 2011;258(5):804–10.PubMed
132.
go back to reference 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(1):51–6.PubMed 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(1):51–6.PubMed
133.
go back to reference Schoenfeld MA, Tempelmann C, Gaul C, Kühnel GR, Düzel E, Hopf J-M, et al. Functional motor compensation in amyotrophic lateral sclerosis. J Neurol. 2005;252(8):944–52.PubMed Schoenfeld MA, Tempelmann C, Gaul C, Kühnel GR, Düzel E, Hopf J-M, et al. Functional motor compensation in amyotrophic lateral sclerosis. J Neurol. 2005;252(8):944–52.PubMed
134.
go back to reference Lule D, Diekmann V, Muller H-P, Kassubek J, Ludolph AC, Birbaumer N. Neuroimaging of multimodal sensory stimulation in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2010;81(8):899–906.PubMed Lule D, Diekmann V, Muller H-P, Kassubek J, Ludolph AC, Birbaumer N. Neuroimaging of multimodal sensory stimulation in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2010;81(8):899–906.PubMed
135.
go back to reference Stoppel CM, Vielhaber S, Eckart C, Machts J, Kaufmann J, Heinze H-J, et al. Structural and functional hallmarks of amyotrophic lateral sclerosis progression in motor- and memory-related brain regions. NeuroImage Clin. 2014;5:277–90.PubMedPubMedCentral Stoppel CM, Vielhaber S, Eckart C, Machts J, Kaufmann J, Heinze H-J, et al. Structural and functional hallmarks of amyotrophic lateral sclerosis progression in motor- and memory-related brain regions. NeuroImage Clin. 2014;5:277–90.PubMedPubMedCentral
136.
go back to reference Jelsone-Swain L, Persad C, Burkard D, Welsh RC. Action Processing and Mirror Neuron Function in Patients with Amyotrophic Lateral Sclerosis: An fMRI Study. Iacoboni M, editor. PLOS ONE. 2015 Apr 17;10(4):e0119862. Jelsone-Swain L, Persad C, Burkard D, Welsh RC. Action Processing and Mirror Neuron Function in Patients with Amyotrophic Lateral Sclerosis: An fMRI Study. Iacoboni M, editor. PLOS ONE. 2015 Apr 17;10(4):e0119862.
137.
go back to reference Bede P, Hardiman O. Lessons of ALS imaging: Pitfalls and future directions - A critical review. NeuroImage Clin. 2014;4:436–43.PubMedPubMedCentral Bede P, Hardiman O. Lessons of ALS imaging: Pitfalls and future directions - A critical review. NeuroImage Clin. 2014;4:436–43.PubMedPubMedCentral
138.
go back to reference Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Mot Neuron Disord Off Publ World Fed Neurol Res Group Mot Neuron Dis. 2000;1(5):293–9. Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Mot Neuron Disord Off Publ World Fed Neurol Res Group Mot Neuron Dis. 2000;1(5):293–9.
139.
go back to reference Andersen PM, Borasio GD, Dengler R, Hardiman O, Kollewe K, Leigh PN, et al. EFNS task force on management of amyotrophic lateral sclerosis: guidelines for diagnosing and clinical care of patients and relatives. Eur J Neurol. 2005;12(12):921–38.PubMed Andersen PM, Borasio GD, Dengler R, Hardiman O, Kollewe K, Leigh PN, et al. EFNS task force on management of amyotrophic lateral sclerosis: guidelines for diagnosing and clinical care of patients and relatives. Eur J Neurol. 2005;12(12):921–38.PubMed
140.
go back to reference Turner MR, Kiernan MC, Leigh PN, Talbot K. Biomarkers in amyotrophic lateral sclerosis. Lancet Neurol. 2009;8(1):94–109.PubMed Turner MR, Kiernan MC, Leigh PN, Talbot K. Biomarkers in amyotrophic lateral sclerosis. Lancet Neurol. 2009;8(1):94–109.PubMed
141.
go back to reference Pradat P-F, Bruneteau G. [Clinical characteristics of amyotrophic lateral sclerosis subsets]. Rev Neurol (Paris). 2006 Jun;162 Spec No 2:4S29-24S33. Pradat P-F, Bruneteau G. [Clinical characteristics of amyotrophic lateral sclerosis subsets]. Rev Neurol (Paris). 2006 Jun;162 Spec No 2:4S29-24S33.
142.
go back to reference Zoccolella S, Beghi E, Palagano G, Fraddosio A, Samarelli V, Lamberti P, et al. Predictors of delay in the diagnosis and clinical trial entry of amyotrophic lateral sclerosis patients: a population-based study. J Neurol Sci. 2006;250(1–2):45–9.PubMed Zoccolella S, Beghi E, Palagano G, Fraddosio A, Samarelli V, Lamberti P, et al. Predictors of delay in the diagnosis and clinical trial entry of amyotrophic lateral sclerosis patients: a population-based study. J Neurol Sci. 2006;250(1–2):45–9.PubMed
143.
go back to reference Pradat P-F, El Mendili M-M. Neuroimaging to investigate multisystem involvement and provide biomarkers in amyotrophic lateral sclerosis. BioMed Res Int. 2014;2014:467560.PubMedPubMedCentral Pradat P-F, El Mendili M-M. Neuroimaging to investigate multisystem involvement and provide biomarkers in amyotrophic lateral sclerosis. BioMed Res Int. 2014;2014:467560.PubMedPubMedCentral
144.
go back to reference 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(5):400–3.PubMed 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(5):400–3.PubMed
145.
go back to reference Filippi M, Agosta F, Grosskreutz J, Benatar M, Kassubek J, Verstraete E, et al. Progress towards a neuroimaging biomarker for amyotrophic lateral sclerosis. Lancet Neurol. 2015;14(8):786–8.PubMed Filippi M, Agosta F, Grosskreutz J, Benatar M, Kassubek J, Verstraete E, et al. Progress towards a neuroimaging biomarker for amyotrophic lateral sclerosis. Lancet Neurol. 2015;14(8):786–8.PubMed
146.
go back to reference Müller H-P, Turner MR, Grosskreutz J, Abrahams S, Bede P, Govind V, et al. A large-scale multicentre cerebral diffusion tensor imaging study in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2016;87(6):570–9.PubMed Müller H-P, Turner MR, Grosskreutz J, Abrahams S, Bede P, Govind V, et al. A large-scale multicentre cerebral diffusion tensor imaging study in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2016;87(6):570–9.PubMed
Metadata
Title
The value of magnetic resonance imaging as a biomarker for amyotrophic lateral sclerosis: a systematic review
Authors
G. Grolez
C. Moreau
V. Danel-Brunaud
C. Delmaire
R. Lopes
P. F. Pradat
M. M. El Mendili
L. Defebvre
D. Devos
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2016
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-016-0672-6

Other articles of this Issue 1/2016

BMC Neurology 1/2016 Go to the issue