Quantitative mapping of T1 and T2 discloses nigral and brainstem pathology in early Parkinson's disease

NeuroImage

Volumn 51, Issue 2, 2010, Pages 512-520

  Baudrexel, Simon ^a   Nürnberger, Lucas ^a   Rüb, Udo ^a   Seifried, Carola ^a   Klein, Johannes C ^a   Deller, Thomas ^a   Steinmetz, Helmuth ^a   Deichmann, Ralf ^a   Hilker, Rüdiger ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Parkinson's disease Quantitative MRI T1 T2

Indexed keywords

ADULT; ARTICLE; BRAIN ASYMMETRY; BRAIN MAPPING; BRAIN STEM; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; MALE; MESENCEPHALON; MOTOR DYSFUNCTION; NIGRONEOSTRIATAL SYSTEM; NUCLEAR MAGNETIC RESONANCE IMAGING; PARKINSON DISEASE; PONS RETICULAR FORMATION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RELAXATION TIME; RIGHT HANDEDNESS; SENSITIVITY AND SPECIFICITY; SUBSTANTIA NIGRA;

EID: 77952100088     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.03.005     Document Type: Article

References (66)

1. Afshar F., Watkins E.S., Yap J.C. Stereotaxic Atlas of the human brainstem and cerebellar nuclei 1978, Raven Press, New York, A Variability Study.
2. Aoe H., Takeda Y., Kawahara H., Tanaka A., Morita K. Clinical significance of T1-weighted MR images following transient cerebral ischemia. J. Neurol. Sci. 2006, 241:19-24.
3. Baudrexel S., Volz S., Preibisch C., Klein J.C., Steinmetz H., Hilker R., Deichmann R. Rapid single-scan T2-mapping using exponential excitation pulses and image-based correction for linear background gradients. Magn. Reson. Med. 2009, 62:263-268.
4. Berg D., Hochstrasser H. Iron metabolism in Parkinsonian syndromes. Mov. Disord. 2006, 21:1299-1310.
5. Berg D., Roggendorf W., Schroder U., Klein R., Tatschner T., Benz P., Tucha O., Preier M., Lange K.W., Reiners K., Gerlach M., Becker G. Echogenicity of the substantia nigra: association with increased iron content and marker for susceptibility to nigrostriatal injury. Arch. Neurol. 2002, 59:999-1005.
6. Berg D., Merz B., Reiners K., Naumann M., Becker G. Five-year follow-up study of hyperechogenicity of the substantia nigra in Parkinson's disease. Mov. Disord. 2005, 20:383-385.
7. Bottomley P.A., Foster T.H., Argersinger R.E., Pfeifer L.M. A review of normal tissue hydrogen NMR relaxation times and relaxation mechanisms from 1-100MHz: dependence on tissue type, NMR frequency, temperature, species, excision, and age. Med. Phys. 1984, 11:425-448.
8. Braak H., de Vos R.A., Jansen E.N., Bratzke H., Braak E. Neuropathological hallmarks of Alzheimer's and Parkinson's diseases. Prog. Brain Res. 1998, 117:267-285.
9. Braak H., Del Tredici K., Rüb U., de Vos R.A., Jansen Steur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 2003, 24:197-211.
10. Brooks D.J. Morphological and functional imaging studies on the diagnosis and progression of Parkinson's disease. J. Neurol. 2000, 247(Suppl. 2):II11-II18.
11. Chaudhuri K.R., Naidu Y. Early Parkinson's disease and non-motor issues. J. Neurol. 2008, 255(Suppl 5):33-38.
12. Chaudhuri K.R., Healy D.G., Schapira A.H. Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurol. 2006, 5:235-245.
13. Corfield D.R., Murphy K., Josephs O., Adams L., Turner R. Does hypercapnia-induced cerebral vasodilation modulate the hemodynamic response to neural activation?. Neuroimage 2001, 13:1207-1211.
14. Croisier E., Graeber M.B. Glial degeneration and reactive gliosis in alpha-synucleinopathies: the emerging concept of primary gliodegeneration. Acta Neuropathol. 2006, 112:517-530.
15. Damier P., Hirsch E.C., Agid Y., Graybiel A.M. The substantia nigra of the human brain: II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain 1999, 122:1437-1448.
16. Deoni S.C., Peters T.M., Rutt B.K. High-resolution T1 and T2 mapping of the brain in a clinically acceptable time with DESPOT1 and DESPOT2. Magn. Reson. Med. 2005, 53:237-241.
17. Dexter D.T., Carayon A., Javoy-Agid F., Agid Y., Wells F.R., Daniel S.E., Lees A.J., Jenner P., Marsden C.D. Alterations in the levels of iron, ferritin and other trace metals in Parkinson's disease and other neurodegenerative diseases affecting the basal ganglia. Brain 1991, 114:1953-1975.
18. Djaldetti R., Shifrin A., Rogowski Z., Sprecher E., Melamed E., Yarnitsky D. Quantitative measurement of pain sensation in patients with Parkinson disease. Neurology 2004, 62:2171-2175.
19. Djaldetti R., Ziv I., Melamed E. The mystery of motor asymmetry in Parkinson's disease. Lancet Neurol. 2006, 5:796-802.
20. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 2005, 25:1325-1335.
21. Enzmann D.R., Pelc N.J. Brain motion: measurement with phase-contrast MR imaging. Radiology 1992, 185:653-660.
22. Fearnley J.M., Lees A.J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 1991, 114:2283-2301.
23. Friston K.J. Testing for anatomically specified regional effects. Hum. Brain Mapp. 1997, 5:133-136.
24. Fusina S., Conte S., Bertolasi L., Fincati E., Nardelli E., Bongiovanni L.G. Sympathetic skin response asymmetry in early stage idiopathic Parkinson's disease. Clin. Neurophysiol. 1999, 110:358-366.
25. Gelman N., Ewing J.R., Gorell J.M., Spickler E.M., Solomon E.G. Interregional variation of longitudinal relaxation rates in human brain at 3.0T: relation to estimated iron and water contents. Magn. Reson. Med. 2001, 45:71-79.
26. Gerhard A., Watts J., Trender-Gerhard I., Turkheimer F., Banati R.B., Bhatia K., Brooks D.J. In vivo imaging of microglial activation with [11C](R)-PK11195 PET in corticobasal degeneration. Mov. Disord. 2004, 19:1221-1226.
27. Gibb W.R., Lees A.J. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 1988, 51:745-752.
28. Gorell J.M., Ordidge R.J., Brown G.G., Deniau J.C., Buderer N.M., Helpern J.A. Increased iron-related MRI contrast in the substantia nigra in Parkinson's disease. Neurology 1995, 45:1138-1143.
29. Götz M.E., Double K., Gerlach M., Youdim M.B., Riederer P. The relevance of iron in the pathogenesis of Parkinson's disease. Ann. N. Y. Acad. Sci. 2004, 1012:193-208.
30. Graham J.M., Paley M.N., Grunewald R.A., Hoggard N., Griffiths P.D. Brain iron deposition in Parkinson's disease imaged using the PRIME magnetic resonance sequence. Brain 2000, 123:2423-2431.
31. Grinberg L.T., Rueb U., Alho A.T., Heinsen H. Brainstem pathology and non-motor symptoms in PD. J. Neurol. Sci. 2009.
32. Harvey A.K., Pattinson K.T., Brooks J.C., Mayhew S.D., Jenkinson M., Wise R.G. Brainstem functional magnetic resonance imaging: disentangling signal from physiological noise. J. Magn. Reson. Imaging 2008, 28:1337-1344.
33. Hirano S., Asanuma K., Ma Y., Tang C., Feigin A., Dhawan V., Carbon M., Eidelberg D. Dissociation of metabolic and neurovascular responses to levodopa in the treatment of Parkinson's disease. J. Neurosci. 2008, 28:4201-4209.
34. Hoehn M.M., Yahr M.D. Parkinsonism: onset, progression and mortality. Neurology 1967, 17:427-442.
35. Hu M.T., White S.J., Herlihy A.H., Chaudhuri K.R., Hajnal J.V., Brooks D.J. A comparison of (18)F-dopa PET and inversion recovery MRI in the diagnosis of Parkinson's disease. Neurology 2001, 56:1195-1200.
36. Hughes A.J., Daniel S.E., Kilford L., Lees A.J. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J. Neurol. Neurosurg. Psychiatry 1992, 55:181-184.
37. Hutchinson M., Raff U. Parkinson's disease: a novel MRI method for determining structural changes in the substantia nigra. J. Neurol. Neurosurg. Psychiatry 1999, 67:815-818.
38. Hutchinson M., Raff U. Structural changes of the substantia nigra in Parkinson's disease as revealed by MR imaging. AJNR Am. J. Neuroradiol. 2000, 21:697-701.
39. Hutchinson M., Raff U. On false negatives in MRI studies of Parkinson disease. Mov. Disord. 2007, 22:1521-1522. author reply 1522.
40. Hutchinson M., Raff U. Detection of Parkinson's disease by MRI: spin-lattice distribution imaging. Mov. Disord. 2008, 23:1991-1997.
41. Imamura K., Hishikawa N., Sawada M., Nagatsu T., Yoshida M., Hashizume Y. Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathol. 2003, 106:518-526.
42. Kempster P.A., Gibb W.R., Stern G.M., Lees A.J. Asymmetry of substantia nigra neuronal loss in Parkinson's disease and its relevance to the mechanism of levodopa related motor fluctuations. J. Neurol. Neurosurg. Psychiatry 1989, 52:72-76.
43. Martin W.R., Wieler M., Gee M. Midbrain iron content in early Parkinson disease: a potential biomarker of disease status. Neurology 2008, 70:1411-1417.
44. McGeer P.L., McGeer E.G. Glial reactions in Parkinson's disease. Mov. Disord. 2008, 23:474-483.
45. Menke R.A., Scholz J., Miller K.L., Deoni S., Jbabdi S., Matthews P.M., Zarei M. MRI characteristics of the substantia nigra in Parkinson's disease: a combined quantitative T1 and DTI study. Neuroimage 2009, 47:435-441.
46. Morrish P.K., Sawle G.V., Brooks D.J. Clinical and [18F] dopa PET findings in early Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 1995, 59:597-600.
47. Munch G., Luth H.J., Wong A., Arendt T., Hirsch E., Ravid R., Riederer P. Crosslinking of alpha-synuclein by advanced glycation endproducts-an early pathophysiological step in Lewy body formation?. J. Chem. Neuroanat. 2000, 20:253-257.
48. Naidich T.P., Duvernoy H.M., Delman B.N., Sorensen A.G., Kollias S.S., Haacke E.M. Duvernoy's Atlas of the Human Brain Stem and Cerebellum: High-Field MRI: Surface Anatomy, Internal Structure, Vascularization and 3D Sectional Anatomy 2009, Springer-Verlag, Wien New York.
49. Napadow V., Dhond R., Kennedy D., Hui K.K., Makris N. Automated brainstem co-registration (ABC) for MRI. Neuroimage 2006, 32:1113-1119.
50. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15:1-25.
51. Oikawa H., Sasaki M., Tamakawa Y., Ehara S., Tohyama K. The substantia nigra in Parkinson disease: proton density-weighted spin-echo and fast short inversion time inversion-recovery MR findings. AJNR Am. J. Neuroradiol. 2002, 23:1747-1756.
52. Ordidge R.J., Gorell J.M., Deniau J.C., Knight R.A., Helpern J.A. Assessment of relative brain iron concentrations using T2-weighted and T2-weighted MRI at 3 Tesla. Magn. Reson. Med. 1994, 32:335-341.
53. Preibisch C., Deichmann R. Influence of RF spoiling on the stability and accuracy of T1 mapping based on spoiled FLASH with varying flip angles. Magn. Reson. Med. 2009, 61:125-135.
54. Preibisch C., Volz S., Anti S., Deichmann R. Exponential excitation pulses for improved water content mapping in the presence of background gradients. Magn. Reson. Med. 2008, 60:908-916.
55. Scherfler C., Schocke M.F., Seppi K., Esterhammer R., Brenneis C., Jaschke W., Wenning G.K., Poewe W. Voxel-wise analysis of diffusion weighted imaging reveals disruption of the olfactory tract in Parkinson's disease. Brain 2006, 129:538-542.
56. Seppi K., Schocke M.F. An update on conventional and advanced magnetic resonance imaging techniques in the differential diagnosis of neurodegenerative parkinsonism. Curr. Opin. Neurol. 2005, 18:370-375.
57. Siemonsen S., Finsterbusch J., Matschke J., Lorenzen A., Ding X.Q., Fiehler J. Age-dependent normal values of T2 and T2' in brain parenchyma. AJNR Am. J. Neuroradiol. 2008, 29:950-955.
58. Sofic E., Paulus W., Jellinger K., Riederer P., Youdim M.B. Selective increase of iron in substantia nigra zona compacta of parkinsonian brains. J. Neurochem. 1991, 56:978-982.
59. Sullivan K.L., Ward C.L., Hauser R.A., Zesiewicz T.A. Prevalence and treatment of non-motor symptoms in Parkinson's disease. Parkinson. Relat. Disord. 2007, 13:545.
60. Uversky V.N., Li J., Fink A.L. Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson's disease and heavy metal exposure. J Biol Chem 2001, 276:44284-44296.
61. Vaillancourt D.E., Spraker M.B., Prodoehl J., Abraham I., Corcos D.M., Zhou X.J., Comella C.L., Little D.M. High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology 2009, 72:1378-1384.
62. Vymazal J., Righini A., Brooks R.A., Canesi M., Mariani C., Leonardi M., Pezzoli G. T1 and T2 in the brain of healthy subjects, patients with Parkinson disease, and patients with multiple system atrophy: relation to iron content. Radiology 1999, 211:489-495.
63. Wallis L.I., Paley M.N., Graham J.M., Grunewald R.A., Wignall E.L., Joy H.M., Griffiths P.D. MRI assessment of basal ganglia iron deposition in Parkinson's disease. J. Magn. Reson. Imaging 2008, 28:1061-1067.
64. Wansapura J.P., Holland S.K., Dunn R.S., Ball W.S. NMR relaxation times in the human brain at 3.0 Tesla. J. Magn. Reson. Imaging 1999, 9:531-538.
65. Yarnykh V.L. Actual flip-angle imaging in the pulsed steady state: a method for rapid three-dimensional mapping of the transmitted radiofrequency field. Magn. Reson. Med. 2007, 57:192-200.
66. Zrinzo L., Zrinzo L.V., Tisch S., Limousin P.D., Yousry T.A., Afshar F., Hariz M.I. Stereotactic localization of the human pedunculopontine nucleus: atlas-based coordinates and validation of a magnetic resonance imaging protocol for direct localization. Brain 2008, 131:1588-1598.