Histological-MRI correlation in the primary motor cortex of patients with amyotrophic lateral sclerosis

Journal of Magnetic Resonance Imaging

Volumn 41, Issue 3, 2015, Pages 665-675

  Meadowcroft, Mark D ^a   Mutic, Nathan J ^a   Bigler, Don C ^a   Wang, Jian Li ^a   Simmons, Zachary ^a   Connor, James R ^a   Yang, Qing X ^a  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

ALS; Amyotrophic lateral sclerosis; Histology; Longitudinal relaxation; Magnetic resonance imaging; MRI; T1

Indexed keywords

BIOLOGICAL MARKER; MYELIN;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN; BRAIN MAPPING; BRAIN TISSUE; CELL COUNT; CELL DENSITY; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION COEFFICIENT; DENSITOMETRY; DIFFUSION WEIGHTED IMAGING; DISEASE SEVERITY; FEMALE; GRAY MATTER; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMAGE ANALYSIS; MALE; MYELIN SHEATH; NERVE FIBER; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PARAMETRIC TEST; PATHOPHYSIOLOGY; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; STRIATE CORTEX; TISSUE SECTION; WHITE MATTER; CADAVER; MIDDLE AGED; MOTOR CORTEX; PATHOLOGY; ULTRASTRUCTURE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AMYOTROPHIC LATERAL SCLEROSIS; CADAVER; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTOR CORTEX;

EID: 84923205644     PISSN: 10531807     EISSN: 15222586     Source Type: Journal    
DOI: 10.1002/jmri.24582     Document Type: Article

References (58)

1. Charil A, Corbo M, Filippi M, et al. Structural and metabolic changes in the brain of patients with upper motor neuron disorders: a multiparametric MRI study. Amyotroph Lateral Scler 2009;10:269-279.
2. Hong YH, Lee KW, Sung JJ, Chang KH, Song IC. Diffusion tensor MRI as a diagnostic tool of upper motor neuron involvement in amyotrophic lateral sclerosis. J Neurol Sci 2004;227:73-78.
3. Williams TL. Motor neurone disease: diagnostic pitfalls. Clin Med 2013;13:97-100.
4. Abe O, Yamada H, Masutani Y, et al. Amyotrophic lateral sclerosis: diffusion tensor tractography and voxel-based analysis. NMR Biomed 2004;17:411-416.
5. Veyrat-Durebex C, Corcia P, Dangoumau A, et al. Advances in cellular models to explore the pathophysiology of amyotrophic lateral sclerosis. Mol Neurobiol 2013. [Epub ahead of print].
6. Andjus PR, Bataveljic D, Vanhoutte G, et al. In vivo morphological changes in animal models of amyotrophic lateral sclerosis and Alzheimer's-like disease: MRI approach. Anat Rec (Hoboken) 2009;292:1882-1892.
7. Paternostro-Sluga T, Grim-Stieger M, Posch M, et al. Reliability and validity of the Medical Research Council (MRC) scale and a modified scale for testing muscle strength in patients with radial palsy. J Rehabil Med 2008;40:665-671.
8. Cedarbaum JM, Stambler N, Malta E, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 1999;169:13-21.
9. 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.
10. Bjarkam CR, Pedersen M, Sorensen JC. New strategies for embedding, orientation and sectioning of small brain specimens enable direct correlation to MR-images, brain atlases, or use of unbiased stereology. J Neurosci Methods [Research Support, Non-U.S. Gov't]. 2001;108:153-159.
11. Fabich HT, Vogt SJ, Sherick ML, et al. Microbial and algal alginate gelation characterized by magnetic resonance. J Biotechnol [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.]. 2012;161:320-327.
12. Riederer SJ, Bobman SA, Lee JN, Farzaneh F, Wang HZ. Improved precision in calculated T1 MR images using multiple spin-echo acquisition. J Comput Assist Tomogr [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.]. 1986;10:103-110.
13. Gupta RK. A new look at the method of variable nutation angle for the measurement of spin-lattice relaxation times using fourier transform NMR. J Magn Reson 1977;25:231-235.
14. Kluver H, Barrera E. A method for the combined staining of cells and fibers in the nervous system. J Neuropathol Exp Neurol 1953;12:400-403.
15. Ostergaard PJ, Jensen MB. Histological quantification of astrocytosis after cerebral infarction: a systematic review. Int J Neurosci [Research Support, N.I.H., Extramural]. 2013;123:439-443.
16. Anderson MA, Ao Y, Sofroniew MV. Heterogeneity of reactive astrocytes. Neurosci Lett 2013. [Epub ahead of print].
17. Sun D, Jakobs TC. Structural remodeling of astrocytes in the injured CNS. Neuroscientist. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review]. 2012;18:567-588.
18. Holmes G. The pathology of amyotrophic lateral sclerosis. Rev Neurol Psychiatry 1909;4:693-724.
19. Davison C. Amyotrophic lateral sclerosis: origin and extent of the upper motor neuron lesion. Arch Neurol Psychiatry 1941;46:1039-1056.
20. Kushner PD, Stephenson DT, Wright S. Reactive astrogliosis is widespread in the subcortical white matter of amyotrophic lateral sclerosis brain. J Neuropathol Exp Neurol 1991;50:263-277.
21. Kamo H, Haebara H, Akiguchi I, Kameyama M, Kimura H, McGeer PL. A distinctive distribution of reactive astroglia in the precentral cortex in amyotrophic lateral sclerosis. Acta Neuropathol 1987;74:33-38.
22. Murayama S, Inoue K, Kawakami H, Bouldin TW, Suzuki K. A unique pattern of astrocytosis in the primary motor area in amyotrophic lateral sclerosis. Acta Neuropathol 1991;82:456-461.
23. Barbeito LH, Pehar M, Cassina P, et al. A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Res Brain Res Rev 2004;47:263-274.
24. Lasiene J, Yamanaka K. Glial cells in amyotrophic lateral sclerosis. Neurol Res Int 2011:718987.
25. Niebroj-Dobosz I, Rafalowska J, Fidzianska A, Gadamski R, Grieb P. Myelin composition of spinal cord in a model of amyotrophic lateral sclerosis (ALS) in SOD1G93A transgenic rats. Folia Neuropathol 2007;45:236-241.
26. Kolind S, Sharma R, Knight S, Johansen-Berg H, Talbot K, Turner MR. Myelin imaging in amyotrophic and primary lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 2013;14:562-573.
27. Janardhan V, Suri S, Bakshi R. Multiple sclerosis: hyperintense lesions in the brain on nonenhanced T1-weighted MR images evidenced as areas of T1 shortening. Radiology 2007;244:823-831.
28. Haimes AB, Zimmerman RD, Morgello S, et al. MR imaging of brain abscesses. AJR Am J Roentgenol 1989;152:1073-1085.
29. de Kerviler E, Cuenod CA, Clement O, et al. [What is bright on T1 MRI scans?]. J Radiol 1998;79:117-126.
30. Terada H, Barkovich AJ, Edwards MS, Ciricillo SM. Evolution of high-intensity basal ganglia lesions on T1-weighted MR in neurofibromatosis type 1. AJNR Am J Neuroradiol 1996;17:755-760.
31. Wansapura JP, Holland SK, Dunn RS, Ball WS Jr. NMR relaxation times in the human brain at 3.0 tesla. J Magn Reson Imaging 1999;9:531-538.
32. Jezzard P, Duewell S, Balaban RS. MR relaxation times in human brain: measurement at 4 T. Radiology [Research Support, Non-U.S. Gov't]. 1996;199:773-779.
33. Fischer HW, Rinck PA, Van Haverbeke Y, Muller RN. Nuclear relaxation of human brain gray and white matter: analysis of field dependence and implications for MRI. Magn Reson Med [Research Support, Non-U.S. Gov't]. 1990;16:317-334.
34. Fujioka M, Taoka T, Matsuo Y, Hiramatsu KI, Sakaki T. Novel brain ischemic change on MRI. Delayed ischemic hyperintensity on T1-weighted images and selective neuronal death in the caudoputamen of rats after brief focal ischemia. Stroke 1999;30:1043-1046.
35. Baheti NN, Cherian A, Wattamwar PR, Kesavadas C, Thomas B. Ischemic hyperintensities on T1-weighted magnetic resonance imaging of patients with stroke: new insights from susceptibility weighted imaging. Neurol India 2010;58:90-94.
36. Shan DE. Delayed ischemic hyperintensity of T1-weighted MRI. Stroke 2000;31:797-798.
37. Fujioka M, Taoka T, Matsuo Y, et al. Delayed ischemic hyperintensity on T1 weighted MRI and induced manganese superoxide dismutase in mitochondria after mild focal ischemia: long-lasting oxidative stress hypothesis. Stroke 2000;31:341.
38. Keller AF, Gravel M, Kriz J. Live imaging of amyotrophic lateral sclerosis pathogenesis: disease onset is characterized by marked induction of GFAP in Schwann cells. Glia 2009;57:1130-1142.
39. Liu D. The roles of free radicals in amyotrophic lateral sclerosis. J Mol Neurosci 1996;7:159-167.
40. Liu D, Wen J, Liu J, Li L. The roles of free radicals in amyotrophic lateral sclerosis: reactive oxygen species and elevated oxidation of protein, DNA, and membrane phospholipids. FASEB J 1999;13:2318-2328.
41. van Waesberghe JH, Kamphorst W, De Groot CJ, et al. Axonal loss in multiple sclerosis lesions: magnetic resonance imaging insights into substrates of disability. Ann Neurol 1999;46:747-754.
42. Schmierer K, Scaravilli F, Altmann DR, Barker GJ, Miller DH. Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain. Ann Neurol 2004;56:407-415.
43. da Rocha AJ, Oliveira AS, Fonseca RB, et al. Detection of corticospinal tract compromise in amyotrophic lateral sclerosis with brain MR imaging: relevance of the T1-weighted spin-echo magnetization transfer contrast sequence. AJNR Am J Neuroradiol 2004;25:1509-1515.
44. Menon RS, Rusinko MS, Allen PS. Proton relaxation studies of water compartmentalization in a model neurological system. Magn Reson Med 1992;28:264-274.
45. Scholtz CL. Quantitative histochemistry of myelin using Luxol Fast Blue MBS. Histochem J 1977;9:759-765.
46. Laule C, Kozlowski P, Leung E, Li DK, Mackay AL, Moore GR. Myelin water imaging of multiple sclerosis at 7 T: correlations with histopathology. Neuroimage 2008;40:1575-1580.
47. Laule C, Leung E, Lis DK, et al. Myelin water imaging in multiple sclerosis: quantitative correlations with histopathology. Mult Scler 2006;12:747-753.
48. Laule C, Vavasour IM, Kolind SH, et al. Magnetic resonance imaging of myelin. Neurotherapeutics 2007;4:460-484.
49. Moore GR, Leung E, MacKay AL, et al. A pathology-MRI study of the short-T2 component in formalin-fixed multiple sclerosis brain. Neurology 2000;55:1506-1510.
50. Nijeholt GJ, Bergers E, Kamphorst W, et al. Post-mortem high-resolution MRI of the spinal cord in multiple sclerosis: a correlative study with conventional MRI, histopathology and clinical phenotype. Brain 2001;124(Pt 1):154-166.
51. Koenig SH, Brown RD III, Spiller M, Lundbom N. Relaxometry of brain: why white matter appears bright in MRI. Magn Reson Med [Research Support, Non-U.S. Gov't]. 1990;14:482-495.
52. Barkovich AJ, Kjos BO, Jackson DE Jr, Norman D. Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. Radiology 1988;166(Pt 1):173-180.
53. Masumura M. Proton relaxation time of immature brain. II. In vivo measurement of proton relaxation time (T1 and T2) in pediatric brain by MRI. Childs Nerv Syst (Case Reports). 1987;3:6-11.
54. Holland BA, Haas DK, Norman D, Brant-Zawadzki M, Newton TH. MRI of normal brain maturation. AJNR Am J Neuroradiol 1986;7:201-208.
55. Deoni SC, Mercure E, Blasi A, et al. Mapping infant brain myelination with magnetic resonance imaging. J Neurosci 2011;31:784-791.
56. Lee Y, Morrison BM, Li Y, et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature [Research Support, N.I.H., Extramural. Research Support, Non-U.S. Gov't]. 2012;487:443-448.
57. Usman U, Choi C, Camicioli R, et al. Mesial prefrontal cortex degeneration in amyotrophic lateral sclerosis: a high-field proton MR spectroscopy study. AJNR Am J Neuroradiol [Controlled Clinical Trial Research Support, Non-U.S. Gov't]. 2011;32:1677-1680.
58. Cosottini M, Cecchi P, Piazza S, et al. Mapping cortical degeneration in ALS with magnetization transfer ratio and voxel-based morphometry. PloS One 2013;8:e68279.