Multi-modal quantitative MRI investigation of brain tissue neurodegeneration in multiple sclerosis

Journal of Magnetic Resonance Imaging

Volumn 35, Issue 6, 2012, Pages 1300-1311

  Hasan, Khader M ^a   Walimuni, Indika S ^a   Abid, Humaira ^a   Wolinsky, Jerry S ^a   Narayana, Ponnada A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

aging; Atlas based; diffusion tensor imaging; FreeSurfer; human brain mapping; lesion mapping; macrostructure; microstructure; Multiple sclerosis; neurodegeneration; quantitative MRI; T2 relaxation; volumetry; Wallerian degeneration

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN ATROPHY; BRAIN CORTEX; BRAIN SIZE; BRAIN TISSUE; CONTROLLED STUDY; CORONA RADIATA (BRAIN); CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; DISABILITY; FEMALE; FRACTIONAL ANISOTROPY; GRAY MATTER; HEALTH INSURANCE; HUMAN; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; NEOCORTEX; NERVE DEGENERATION; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROSPECTIVE STUDY; QUANTITATIVE ANALYSIS; RELAPSE; REMISSION; RHOMBENCEPHALIC ISTHMUS; THALAMUS; WHITE MATTER;

ADULT; BRAIN; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; NEURODEGENERATIVE DISEASES; RECURRENCE; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SUBTRACTION TECHNIQUE;

EID: 84862080666     PISSN: 10531807     EISSN: 15222586     Source Type: Journal    
DOI: 10.1002/jmri.23539     Document Type: Article

References (62)

1. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L,. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998; 338: 278-285. (Pubitemid 28065253)
2. Seewann A, Vrenken H, van der Valk P, et al. Diffusely abnormal white matter in chronic multiple sclerosis: imaging and histopathologic analysis. Arch Neurol 2009; 66: 601-609.
3. Young IR, Hall AS, Pallis CA, Legg NJ, Bydder GM, Steiner RE,. Nuclear magnetic resonance imaging of the brain in multiple sclerosis. Lancet 1981; 2: 1063-1066. (Pubitemid 11026868)
4. Goodin DS,. Magnetic resonance imaging as a surrogate outcome measure of disability in multiple sclerosis: have we been overly harsh in our assessment? (review). Ann Neurol 2006; 59: 597-605.
5. Filippi M, Agosta F,. Imaging biomarkers in multiple sclerosis (review). J Magn Reson Imaging 2010; 31: 770-788.
6. Barkhof F,. The clinico-radiological paradox in multiple sclerosis revisited. (review). Curr Opin Neurol 2002; 15: 239-245. (Pubitemid 34596884)
7. Ramasamy DP, Benedict RH, Cox JL, et al. Extent of cerebellum, subcortical and cortical atrophy in patients with MS: a case-control study. J Neurol Sci 2009; 282: 47-54.
8. Hasan KM, Halphen C, Kamali A, Nelson FM, Wolinsky JS, Narayana PA,. Caudate nuclei volume, diffusion tensor metrics, and T(2) relaxation in healthy adults and relapsing-remitting multiple sclerosis patients: implications for understanding gray matter degeneration. J Magn Reson Imaging 2009; 29: 70-77.
9. Whittall KP, MacKay AL, Li DK, Vavasour IM, Jones CK, Paty DW,. Normal-appearing white matter in multiple sclerosis has heterogeneous, diffusely prolonged T(2). Magn Reson Med 2002; 47: 403-408. (Pubitemid 34116812)
10. Neema M, Goldberg-Zimring D, Guss ZD, et al. 3 T MRI relaxometry detects T2 prolongation in the cerebral normal-appearing white matter in multiple sclerosis. Neuroimage 2009; 46: 633-641.
11. Rocca MA, Pagani E, Absinta M, et al. Altered functional and structural connectivities in patients with MS: a 3-T study. Neurology 2007; 69: 2136-2145. (Pubitemid 350294694)
12. Inglese M, Bester M,. Diffusion imaging in multiple sclerosis: research and clinical implications. NMR Biomed 2010; 23: 865-872.
13. Brass SD, Chen NK, Mulkern RV, Bakshi R,. Magnetic resonance imaging of iron deposition in neurological disorders (review). Top Magn Reson Imaging 2006; 17: 31-40. (Pubitemid 46672931)
14. Song SK, Yoshino J, Le TQ, et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005; 26: 132-140. (Pubitemid 40602893)
15. Kinoshita Y, Ohnishi A, Kohshi K, Yokota A,. Apparent diffusion coefficient on rat brain and nerves intoxicated with methylmercury. Environ Res 1999; 80: 348-354. (Pubitemid 29218357)
16. Beaulieu C,. The basis of anisotropic water diffusion in the nervous system-a technical review (review). NMR Biomed 2002; 15: 435-455. (Pubitemid 36054508)
17. Trapp BD, Nave KA,. Multiple sclerosis: an immune or neurodegenerative disorder? (review). Annu Rev Neurosci 2008; 31: 247-269.
18. Lassmann, H,. Multiple sclerosis: is there neurodegeneration independent from inflammation? J Neurol Sci 2007; 259: 3-6. (Pubitemid 47031195)
19. Chard D, Miller D,. Is multiple sclerosis a generalized disease of the central nervous system? An MRI perspective. Curr Opin Neurol 2009; 22: 214-218.
20. Charil A, Filippi M,. Inflammatory demyelination and neurodegeneration in early multiple sclerosis. J Neural Sci 2007; 259: 7-15. (Pubitemid 47031196)
21. Hasan KM, Kamali A, Rollins NK,. The need for spatially standardized methods in clinical applications of diffusion tensor imaging of white matter. Radiology 2009; 253: 571-572.
22. Janardhan V, Bakshi R,. Quality of life and its relationship to brain lesions and atrophy on magnetic resonance images in 60 patients with multiple sclerosis. Arch Neurol 2000; 57: 1485-1491.
23. Fischl B, Salat DH, Busa E, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002; 33: 341-355. (Pubitemid 34162530)
24. Hasan KM,. A framework for quality control and parameter optimization in diffusion tensor imaging: theoretical analysis and validation. Magn Reson Imaging 2007; 25: 1196-1202. (Pubitemid 47464845)
25. Courchesne E, Chisum HJ, Townsend J, et al. Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology 2000; 216: 672-682. (Pubitemid 30660837)
26. Walimuni IS, Abid H, Hasan KM,. A computational framework to quantify tissue microstructural integrity using conventional MRI macrostructural volumetry. Comput Biol Med 2011; 41: 1073-1081.
27. Desikan RS, Segonne F, Fischl B, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006; 31: 968-980. (Pubitemid 44183792)
28. Aubert-Broche B, Grova C, Pike GB, Collins DL,. Clustering of atlas-defined cortical regions based on relaxation times and proton density. Neuroimage 2009; 47: 523-532.
29. Sajja BR, Datta S, He R, et al. Unified approach for multiple sclerosis lesion segmentation on brain MRI. Ann Biomed Eng 2006; 34: 142-151.
30. Narayanan S, Fu L, Pioro E, et al. Imaging of axonal damage in multiple sclerosis: spatial distribution of magnetic resonance imaging lesions. Ann Neurol 1997; 41: 385-391. (Pubitemid 27114050)
31. Zijdenbos AP, Forghani R, Evans AC,. Automatic "pipeline" analysis of 3-D MRI data for clinical trials: application to multiple sclerosis. IEEE Trans Med Imaging 2002; 21: 1280-1291.
32. Charil A, Dagher A, Lerch JP, Zijdenbos AP, Worsley KJ, Evans AC,. Focal cortical atrophy in multiple sclerosis: relation to lesion load and disability. Neuroimage 2007; 34: 509-517. (Pubitemid 44827772)
33. Vellinga MM, Geurts JJ, Rostrup E, et al. Clinical correlations of brain lesion distribution in multiple sclerosis. J Magn Reson Imaging 2009; 29: 768-773.
34. Brett M, Leff AP, Rorden C, Ashburner J,. Spatial normalization of brain images with focal lesions using cost function masking. Neuroimage 2001; 14: 486-500. (Pubitemid 32709562)
35. Pagani E, Filippi M, Rocca MA, Horsfield MA,. A method for obtaining tract-specific diffusion tensor MRI measurements in the presence of disease: application to patients with clinically isolated syndromes suggestive of multiple sclerosis. Neuroimage 2005; 26: 258-265. (Pubitemid 40602905)
36. Fu L, Wolfson C, Worsley KJ, et al. Statistics for investigation of multimodal MR imaging data and an application to multiple sclerosis patients. NMR Biomed 1996; 9: 339-346. (Pubitemid 27249501)
37. Zou KH, Tuncali K, Silverman SG,. Correlation and simple linear regression. Radiology 2003; 227: 617-622. (Pubitemid 36583011)
38. Sailer M, Fischl B, Salat D, et al. Focal thinning of the cerebral cortex in multiple sclerosis. Brain 2003; 126: 1734-1744. (Pubitemid 36917333)
39. Hasan KM, Walimuni IS, Kramer LA, Frye RE,. Human brain atlas-based volumetry and relaxometry: application to healthy development and natural aging. Magn Reson Med 2010; 64: 1382-1389.
40. Georgiades CS, Itoh R, Golay X, van Zijl PC, Melhem ER,. MR imaging of the human brain at 1.5 T: regional variations in transverse relaxation rates in the cerebral cortex. AJNR Am J Neuroradiol 2001; 22: 1732-1737. (Pubitemid 32999584)
41. Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G,. Diffusion tensor MR imaging of the human brain. Radiology 1996; 201: 637-648.
42. Castriota-Scanderbeg A, Fasano F, Hagberg G, Nocentini U, Filippi M, Caltagirone C,. Coefficient (Dav) is more sensitive than fractional anisotropy in monitoring progression of irreversible tissue damage in focal nonactive multiple sclerosis lesions. AJNR Am J Neuroradiol 2003; 24: 663-670. (Pubitemid 36460737)
43. Mukherjee P, Miller JH, Shimony JS, et al. Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. AJNR Am J Neuroradiol 2002; 23: 1445-1456. (Pubitemid 35154982)
44. Filippi M, Rocca MA,. MRI evidence for multiple sclerosis as a diffuse disease of the central nervous system (review). J Neurol 2005; 252: v16-v24. (Pubitemid 41532351)
45. Vrenken H, Pouwels PJ, Geurts JJ, et al. Altered diffusion tensor in multiple sclerosis normal-appearing brain tissue: cortical diffusion changes seem related to clinical deterioration. J Magn Reson Imaging 2006; 23: 628-636.
46. Evangelou N, Esiri MM, Smith S, Palace J, Matthews PM,. Quantitative pathological evidence for axonal loss in normal appearing white matter in multiple sclerosis. Ann Neurol 2000; 47: 391-395. (Pubitemid 30141854)
47. Wegner C, Esiri MM, Chance SA, Palace J, Matthews PM,. Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology 2006; 67: 960-967. (Pubitemid 44454585)
48. Brooks DJ, Leenders KL, Head G, Marshall J, Legg NJ, Jones T,. Studies on regional cerebral oxygen utilisation and cognitive function in multiple sclerosis. J Neurol Neurosurg Psychiatry 1984; 47: 1182-1191. (Pubitemid 15204531)
49. Blinkenberg M, Rune K, Jensen CV, et al. Cortical cerebral metabolism correlates with MRI lesion load and cognitive dysfunction in MS. Neurology 2000; 54: 558-564. (Pubitemid 30082918)
50. Bakshi R, Miletich RS, Kinkel PR, Emmet ML, Kinkel WR,. High-resolution fluorodeoxyglucose positron emission tomography shows both global and regional cerebral hypometabolism in multiple sclerosis. J Neuroimaging 1998; 8: 228-234. (Pubitemid 28457989)
51. Brownell B, Hughes JT,. The distribution of plaques in the cerebrum in multiple sclerosis. J Neurol Neurosurg Psychiatry 1962; 25: 315-320.
52. Aboitiz F, Scheibel AB, Fisher RS, Zaidel E,. Fiber composition of the human corpus callosum. Brain Res 1992; 598: 143-153. (Pubitemid 23013055)
53. Cader S, Johansen-Berg H, Wylezinska M, et al. Discordant white matter N-acetylasparate and diffusion MRI measures suggest that chronic metabolic dysfunction contributes to axonal pathology in multiple sclerosis Neuroimage 2007; 36: 19-27. (Pubitemid 46617958)
54. Ciccarelli O, Werring DJ, Barker GJ, et al. A study of the mechanisms of normal-appearing white matter damage in multiple sclerosis using diffusion tensor imaging-evidence of Wallerian degeneration. J Neurol 2003; 250: 287-292. (Pubitemid 36399267)
55. Rosas HD, Liu AK, Hersch S, et al. Regional and progressive thinning of the cortical ribbon in Huntington's disease. Neurology 2002; 58: 695-701. (Pubitemid 34211546)
56. Derakhshan M, Caramanos Z, Giacomini PS, et al. Evaluation of automated techniques for the quantification of grey matter atrophy in patients with multiple sclerosis. Neuroimage 2010; 52: 1261-1267.
57. Pellicano C, Gallo A, Li X, et al. Relationship of cortical atrophy to fatigue in patients with multiple sclerosis. Arch Neurol 2010; 67: 447-453.
58. Hasan KM, Walimuni IS, Humaira A, Datta S, Wolinsky JS, Narayana PA,. Human brain atlas-based multimodal MRI analysis of volumetry, diffusimetry, relaxometry and lesion distribution in multiple sclerosis patients and healthy adult controls: implications for understanding the pathogenesis of multiple sclerosis and consolidation of quantitative MRI results in MS. J Neurol Sci 2011 [Epub ahead of print]. DOI: 10.1016/j.jns.2011.09.015.
59. Hasan KM, Walimuni IS, Humaira A, et al. Multimodal quantitative magnetic resonance imaging of thalamic development and aging across the human lifespan: implications to neurodegeneration in multiple sclerosis. J Neurosci 2011; 31: 16826-16832.
60. Walimuni IS, Hasan KM,. Atlas-based investigation of human brain tissue microstructural spatial heterogeneity and interplay between transverse relaxation time and radial diffusivity. Neuroimage 57: 1402-1410.
61. Hasan KM, Walimuni IS, Kramer LA, Narayana PA,. Human brain iron mapping using atlas-based T(2) relaxometry. Magn Reson Med 2011 [Epub ahead of print]. DOI: 10.1002/mrm.23054.
62. Moraal B, Roosendaal SD, Pouwels PJ, et al. Multi-contrast, isotropic, single-slab 3D MR imaging in multiple sclerosis. Eur Radiol 2008; 18: 2311-2320.