Assessment of lesion pathology in a new animal model of MS by multiparametric MRI and DTI

NeuroImage

Volumn 59, Issue 3, 2012, Pages 2678-2688

  Boretius, Susann ^a,c   Escher, Angelika ^b   Dallenga, Tobias ^b   Wrzos, Claudia ^b   Tammer, Roland ^a,c   Brück, Wolfgang ^b,c   Nessler, Stefan ^b   Frahm, Jens ^a,c   Stadelmann, Christine ^b,c  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c Deutsche Forschungsgemeinschaft   (Germany)

Author keywords

Cuprizone; Diffusion tensor imaging (DTI); EAE; Magnetic resonance imaging (MRI); Multiple sclerosis (MS)

Indexed keywords

CUPRIZONE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; BLOOD BRAIN BARRIER; BRAIN DAMAGE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DEMYELINATING DISEASE; DIFFUSION TENSOR IMAGING; DISCRIMINANT ANALYSIS; DISEASE COURSE; ENCEPHALITIS; FEMALE; HISTOPATHOLOGY; IMAGE ANALYSIS; LYMPHOCYTIC INFILTRATION; MOUSE; MULTIPLE SCLEROSIS; NEUROPATHOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL;

ANIMALS; AXONS; BLOOD-BRAIN BARRIER; BRAIN; CUPRIZONE; DEMYELINATING DISEASES; DIFFUSION TENSOR IMAGING; DISCRIMINANT ANALYSIS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GLIOSIS; IMAGE PROCESSING, COMPUTER-ASSISTED; INFLAMMATION; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED C57BL; MONOAMINE OXIDASE INHIBITORS; MULTIPLE SCLEROSIS; PERTUSSIS TOXIN;

EID: 84855425434     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.08.051     Document Type: Article

References (43)

1. Alexander A.L., Lee J.E., Lazar M., Field A.S. Diffusion tensor imaging of the brain. Neurotherapeutics 2007, 4:316-329.
2. Backhaus K., Erichson B., Plinke W., Weiber R. Multivariate Analysemethoden 2003, 192-196. Springer, Berlin.
3. Bakker D.A., Ludwin S.K. Blood-brain barrier permeability during Cuprizone-induced demyelination. Implications for the pathogenesis of immune-mediated demyelinating diseases. J. Neurol. Sci. 1987, 78:125-137.
4. Bammer R., Augustin M., Strasser-Fuchs S., Seifert T., Kapeller P., Stollberger R., et al. Magnetic resonance diffusion tensor imaging for characterizing diffuse and focal white matter abnormalities in multiple sclerosis. Magn. Reson. Med. 2000, 44:583-591.
5. Barkhof F. The clinico-radiological paradox in multiple sclerosis revisited. Curr. Opin. Neurol. 2002, 15:239-245.
6. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 2002, 15:435-455.
7. Beaulieu C., Allen P.S. Water diffusion in the giant axon of the squid: implications for diffusion-weighted MRI of the nervous system. Magn. Reson. Med. 1994, 32:579-583.
8. Boretius S., Gadjanski I., Demmer I., Bahr M., Diem R., Michaelis T., et al. MRI of optic neuritis in a rat model. Neuroimage 2008, 41:323-334.
9. Boretius S., Kasper L., Tammer R., Michaelis T., Frahm J. MRI of cellular layers in mouse brain in vivo. Neuroimage 2009, 47:1252-1260.
10. Bruck W., Bitsch A., Kolenda H., Bruck Y., Stiefel M., Lassmann H. Inflammatory central nervous system demyelination: correlation of magnetic resonance imaging findings with lesion pathology. Ann. Neurol. 1997, 42:783-793.
11. Budde M.D., Kim J.H., Liang H.F., Russell J.H., Cross A.H., Song S.K. Axonal injury detected by in vivo diffusion tensor imaging correlates with neurological disability in a mouse model of multiple sclerosis. NMR Biomed. 2008, 21:589-597.
12. Cheng Y., Chou K.H., Chen I.Y., Fan Y.T., Decety J., Lin C.P. Atypical development of white matter microstructure in adolescents with autism spectrum disorders. Neuroimage 2010, 15:873-882.
13. Ciccarelli O., Werring D.J., Wheeler-Kingshott C.A., Barker G.J., Parker G.J., Thompson A.J., et al. Investigation of MS normal-appearing brain using diffusion tensor MRI with clinical correlations. Neurology 2001, 56:926-933.
14. DeBoy C.A., Zhang J., Dike S., Shats I., Jones M., Reich D.S., et al. High resolution diffusion tensor imaging of axonal damage in focal inflammatory and demyelinating lesions in rat spinal cord. Brain 2007, 130:2199-2210.
15. Dousset V., Grossman R.I., Ramer K.N., Schnall M.D., Young L.H., Gonzalez-Scarano F., et al. Experimental allergic encephalomyelitis and multiple sclerosis: lesion characterization with magnetization transfer imaging. Radiology 1992, 182:483-491.
16. Filippi M., Cercignani M., Inglese M., Horsfield M.A., Comi G. Diffusion tensor magnetic resonance imaging in multiple sclerosis. Neurology 2001, 56:304-311.
17. Giorgio A., Palace J., Johansen-Berg H., Smith S.M., Ropele S., Fuchs S., et al. Relationships of brain white matter microstructure with clinical and MR measures in relapsing-remitting multiple sclerosis. J. Magn. Reson. Imaging 2010, 31:309-316.
18. Hall S.M. The effect of injections of lysophosphatidyl choline into white matter of the adult mouse spinal cord. J. Cell Sci. 1972, 10:535-546.
19. Kondo A., Nakano T., Suzuki K. Blood-brain barrier permeability to horseradish peroxidase in twitcher and Cuprizone-intoxicated mice. Brain Res. 1987, 425:186-190.
20. Kubicki M., McCarley R., Westin C.F., Park H.J., Maier S., Kikinis R., et al. A review of diffusion tensor imaging studies in schizophrenia. J. Psychiatr. Res. 2007, 41:15-30.
21. Lowe M.J., Horenstein C., Hirsch J.G., Marrie R.A., Stone L., Bhattacharyya P.K., et al. Functional pathway-defined MRI diffusion measures reveal increased transverse diffusivity of water in multiple sclerosis. Neuroimage 2006, 32:1127-1133.
22. MacDonald C.L., Dikranian K., Bayly P., Holtzman D., Brody D. Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J. Neurosci. 2007, 27:11869-11876.
23. Matsushima G.K., Morell P. The neurotoxicant, Cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol. 2001, 11:107-116.
24. Merkler D., Boretius S., Stadelmann C., Ernsting T., Michaelis T., Frahm J., et al. Multicontrast MRI of remyelination in the central nervous system. NMR Biomed. 2005, 18:395-403.
25. Nessler S., Boretius S., Stadelmann C., Bittner A., Merkler D., Hartung H.P., et al. Early MRI changes in a mouse model of multiple sclerosis are predictive of severe inflammatory tissue damage. Brain 2007, 130:2186-2198.
26. Pierpaoli C., Barnett A., Pajevic S., Chen R., Penix L.R., Virta A., et al. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 2001, 13:1174-1185.
27. Rausch M., Hiestand P., Baumann D., Cannet C., Rudin M. MRI-based monitoring of inflammation and tissue damage in acute and chronic relapsing EAE. Magn. Reson. Med. 2003, 50:309-314.
28. Riley J.D., Franklin D.L., Choi V., Kim R.C., Binder D.K., Cramer S.C., et al. Altered white matter integrity in temporal lobe epilepsy: association with cognitive and clinical profiles. Epilepsia 2010, 51:536-545.
29. Roosendaal S.D., Geurts J.J., Vrenken H., Hulst H.E., Cover K.S., Castelijns J.A., et al. Regional DTI differences in multiple sclerosis patients. Neuroimage 2009, 44:1397-1403.
30. Schmierer K., Scaravilli F., Altmann D.R., Barker G.J., Miller D.H. Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain. Ann. Neurol. 2004, 56:407-415.
31. Seewann A., Vrenken H., van der Valk P., Blezer E.L., Knol D.L., Castelijns J.A., et al. Diffusely abnormal white matter in chronic multiple sclerosis: imaging and histopathologic analysis. Arch. Neurol. 2009, 66:601-609.
32. Shamy J.L., Carpenter D.M., Fong S.G., Murray E.A., Tang C.Y., Hof P.R., et al. Alterations of white matter tracts following neurotoxic hippocampal lesions in macaque monkeys: A diffusion tensor imaging study. Hippocampus 2010, 20:906-910.
33. Song S.K., Sun S.W., Ju W.K., Lin S.J., Cross A.H., Neufeld A.H. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 2003, 20:1714-1722.
34. Song S.K., Sun S.W., Ramsbottom M.J., Chang C., Russell J., Cross A.H. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 2002, 17:1429-1436.
35. Song S.K., Yoshino J., Le T.Q., Lin S.J., Sun S.W., Cross A.H., et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005, 26:132-140.
36. Stebbins G.T., Murphy C.M. Diffusion tensor imaging in Alzheimer's disease and mild cognitive impairment. Behav. Neurol. 2009, 21:39-49.
37. Sun S.W., Liang H.F., Schmidt R.E., Cross A.H., Song S.K. Selective vulnerability of cerebral white matter in a murine model of multiple sclerosis detected using diffusion tensor imaging. Neurobiol. Dis. 2007, 28:30-38.
38. Sun S.W., Liang H.F., Trinkaus K., Cross A.H., Armstrong R.C., Song S.K. Noninvasive detection of Cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn. Reson. Med. 2006, 55:302-308.
39. van Waesberghe J.H., Kamphorst W., De Groot C.J., van Walderveen M.A., Castelijns J.A., Ravid R., et al. Axonal loss in multiple sclerosis lesions: magnetic resonance imaging insights into substrates of disability. Ann. Neurol. 1999, 46:747-754.
40. Werring D.J., Brassat D., Droogan A.G., Clark C.A., Symms M.R., Barker G.J., et al. The pathogenesis of lesions and normal-appearing white matter changes in multiple sclerosis: a serial diffusion MRI study. Brain 2000, 123(Pt 8):1667-1676.
41. Werring D.J., Clark C.A., Barker G.J., Thompson A.J., Miller D.H. Diffusion tensor imaging of lesions and normal-appearing white matter in multiple sclerosis. Neurology 1999, 52:1626-1632.
42. Wheeler-Kingshott C.A., Cercignani M. About "axial" and "radial" diffusivities. Magn. Reson. Med. 2009, 61:1255-1260.
43. Wu Q., Butzkueven H., Gresle M., Kirchhoff F., Friedhuber A., Yang Q., et al. MR diffusion changes correlate with ultra-structurally defined axonal degeneration in murine optic nerve. Neuroimage 2007, 37:1138-1147.