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High-Field Neuroimaging in Parkinson’s Disease

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High Field Brain MRI

Abstract

Diagnosis and follow-up of Parkinson’s disease (PD) are still essentially based on clinical criteria. At the early stages of the disease, conventional MRI examination may be negative to any visible tissue alteration and, due to its scarce specificity, it is in fact limited to gross differential diagnosis with other neurological disorders. In this chapter, we discuss the potential of using more advanced quantification techniques at 3.0 T and the advantages and drawbacks of 7.0 T magnetic fields in PD.

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References

  1. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381

    Article  CAS  PubMed  Google Scholar 

  3. Youdim MB, Riederer P (2004) A review about brain iron in normal and pathological conditions. In: Encyclopedia of neuroscience. Elsevier, Amsterdam

    Google Scholar 

  4. Zecca L, Youdim MB, Riederer P et al (2004) Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci 5:863–873

    Article  CAS  PubMed  Google Scholar 

  5. Hutchinson M, Raff U (2000) Structural changes of the substantia nigra in Parkinson’s disease as revealed by MR imaging. Am J Neuroradiol 21:697–701

    CAS  PubMed  Google Scholar 

  6. Hutchinson M, Raff U, Lebedev S (2003) MRI correlates of pathology in parkinsonism: segmented inversion recovery ratio imaging (SIRRIM). Neuroimage 20:1899–1902

    Article  PubMed  Google Scholar 

  7. Hu MT, White SJ, Herlihy AH et al (2001) A comparison of (18)F-dopa PET and inversion recovery MRI in the diagnosis of Parkinson’s disease. Neurology 56:1195–1200

    Article  CAS  PubMed  Google Scholar 

  8. Oikawa H, Sasaki M, Tamakawa Y et al (2002) The substantia nigra in Parkinson disease: proton density-weighted spin-echo and fast short inversion time inversion-recovery MR findings. Am J Neuroradiol 23:1747–1756

    PubMed  Google Scholar 

  9. Adachi M, Hosoya T, Haku T et al (1999) Evaluation of the substantia nigra in patients with Parkinsonian syndrome accomplished using multishot diffusion-weighted MR imaging. Am J Neuroradiol 20:1500–1506

    CAS  PubMed  Google Scholar 

  10. Schocke MF, Seppi K, Esterhammer R et al (2004) Trace of diffusion tensor differentiates the Parkinson variant of multiple system atrophy and Parkinson’s disease. Neuroimage 21:1443–1451

    Article  PubMed  Google Scholar 

  11. Eckert T, Sailer M, Kaufmann J et al (2004) Differentiation of idiopathic Parkinson’s disease, multiple system atrophy, progressive supranuclear palsy, and healthy controls using magnetization transfer imaging. Neuroimage 21:229–235

    Article  PubMed  Google Scholar 

  12. Bartzokis G, Cummings JL, Markham CH et al (1999) MRI evaluation of brain iron in earlier- and later-onset Parkinson’s disease and normal subjects. Magn Reson Imaging 17:213–222

    Article  CAS  PubMed  Google Scholar 

  13. Graham JM, Paley MN, Grunewald RA et al (2000) Brain iron deposition in Parkinson’s disease imaged using the PRIME magnetic resonance sequence. Brain 123(12):2423–2431

    Article  PubMed  Google Scholar 

  14. Lehéricy S, Bardinet E, Poupon C et al (2014) 7 tesla magnetic resonance imaging: a closer look at substantia nigra anatomy in Parkinson’s disease. Mov Disord 29(13):1574–1581

    Article  PubMed  Google Scholar 

  15. Menke RA, Scholz J, Miller KL et al (2009) MRI characteristics of the substantia nigra in Parkinson’s disease: a combined quantitative T1 and DTI study. Neuroimage 47(2):435–441

    Article  PubMed  Google Scholar 

  16. Baudrexel S, Nürnberger L, Rüb U et al (2010) Quantitative mapping of T1 and T2* discloses nigral and brainstem pathology in early Parkinson’s disease. Neuroimage 51(2):512–520

    Article  PubMed  Google Scholar 

  17. Peran P, Cherubini A, Assogna F et al (2010) Magnetic resonance imaging markers of Parkinson’s disease nigrostriatal signature. Brain J Neurology 133(11):3423–3433

    Article  Google Scholar 

  18. Murty VP, Shermohammed M, Smith DV et al (2014) Resting state networks distinguish human ventral tegmental area from substantia nigra. Neuroimage 100(C):580–589

    Article  PubMed  PubMed Central  Google Scholar 

  19. Menke RA, Jbabdi S, Miller KL et al (2010) Connectivity-based segmentation of the substantia nigra in human and its implications in Parkinson’s disease. Neuroimage 52:1175–1180

    Article  PubMed  Google Scholar 

  20. Double KL, Gerlach M, Schunemann V et al (2003) Iron-binding charactestics of neuromelanin of the human substantia nigra. Biochem Pharmacol 66:489–494

    Article  CAS  PubMed  Google Scholar 

  21. Sasaki M, Shibata E, Tohyama K et al (2006) Neuromelanin magnetic resonance imaging of locus coeruleus and substantia nigra in Parkinson’s disease. Neuroreport 17:1215–1218

    Article  PubMed  Google Scholar 

  22. Sasaki M, Shibata E, Kudo K et al (2008) Neuromelanin sensitive MRI. Clin Neuroradiol 18:147–153

    Article  Google Scholar 

  23. Reimão S, Pita Lobo P, Neutel D et al (2015) Substantia nigra neuromelanin magnetic resonance imaging in de novo Parkinson’s disease patients. Eur J Neurol 22(3):540–546

    Article  PubMed  Google Scholar 

  24. Kashihara K, Shinya T, Higaki F (2011) Neuromelanin magnetic resonance imaging of nigral volume loss in patients with Parkinson’s disease. J Clin Neurosci 18:1093–1096

    Article  PubMed  Google Scholar 

  25. Eapen M, Zald DH, Gatenby JC et al (2011) Using high-resolution MR imaging at 7 T to evaluate the anatomy of the midbrain dopaminergic system. AJNR Am J Neuroradiol 32(4):688–694

    Article  CAS  PubMed  Google Scholar 

  26. Damier P, Hirsch EC, Agid Y et al (1999) The substantia nigra of the human brain. I. Nigrosomes and the nigral matrix, a compartmental organization based on calbindin D(28 K) immunohistochemistry. Brain 122(Pt 8):1421–1436

    Article  PubMed  Google Scholar 

  27. Damier P, Hirsch EC, Agid Y et al (1999) The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson’s disease. Brain 122(Pt 8):1437–1448

    Article  PubMed  Google Scholar 

  28. Kwon DH, Kim JM, Oh SH et al (2012) Seven-Tesla magnetic resonance images of the substantia nigra in Parkinson disease. Ann Neurol 71:267–277

    Article  PubMed  Google Scholar 

  29. Blazejewska AI, Schwarz ST, Pitiot A et al (2013) Visualization of nigrosome 1 and its loss in PD: pathoanatomical correlation and in vivo 7 T MRI. Neurology 81:534–540

    Article  PubMed  PubMed Central  Google Scholar 

  30. Cosottini M, Frosini D, Pesaresi I et al (2014) MR imaging of the substantia nigra at 7 T enables diagnosis of Parkinson disease. Radiology 271(3):831–838

    Article  PubMed  Google Scholar 

  31. Schwarz ST, Afzal M, Morgan PS et al (2014) The ‘swallow tail’ appearance of the healthy nigrosome: a new accurate test of Parkinson’s disease: a case-control and retrospective cross-sectional MRI study at 3 T. PLoS One 9:e93814

    Article  PubMed  PubMed Central  Google Scholar 

  32. Mueller C, Pinter B, Reiter E et al (2014) Visualization of nigrosome 1 and its loss in PD: pathoanatomical correlation and in vivo 7 T MRI. Neurology 82:1752

    Article  PubMed  Google Scholar 

  33. Brooks DJ (2004) Neuroimaging in Parkinson’s disease. NeuroRx 1:243–254

    Article  PubMed  PubMed Central  Google Scholar 

  34. Ye FQ, Allen PS, Martin WR (1996) Basal ganglia iron content in Parkinson’s disease measured with magnetic resonance. Mov Disord 11:243–249

    Article  CAS  PubMed  Google Scholar 

  35. Antonini A, Leenders KL, Meier D et al (1993) T2 relaxation time in patients with Parkinson’s disease. Neurology 43:697–700

    Article  CAS  PubMed  Google Scholar 

  36. Ryvlin P, Broussolle E, Piollet H et al (1995) Magnetic resonance imaging evidence of decreased putamenal iron content in idiopathic Parkinson’s disease. Arch Neurol 52:583–588

    Article  CAS  PubMed  Google Scholar 

  37. Kosta P, Argyropoulou MI, Markoula S et al (2006) MRI evaluation of the basal ganglia size and iron content in patients with Parkinson’s disease. J Neurol 253(1):26–32

    Article  PubMed  Google Scholar 

  38. Schocke MF, Seppi K, Esterhammer R et al (2002) Diffusion-weighted MRI differentiates the Parkinson variant of multiple system atrophy from PD. Neurology 58:575–580

    Article  CAS  PubMed  Google Scholar 

  39. Seppi K, Schocke MF, Donnemiller E et al (2004) Comparison of diffusion-weighted imaging and [123I]IBZM-SPECT for the differentiation of patients with the Parkinson variant of multiple system atrophy from those with Parkinson’s disease. Mov Disord 19:1438–1445

    Article  PubMed  Google Scholar 

  40. Seppi K, Schocke MF, Esterhammer R et al (2003) Diffusion-weighted imaging discriminates progressive supranuclear palsy from PD, but not from the Parkinson variant of multiple system atrophy. Neurology 60:922–927

    Article  CAS  PubMed  Google Scholar 

  41. Carlesimo GA, Piras F, Assogna F et al (2012) Hippocampal abnormalities and memory deficits in Parkinson disease: a multimodal imaging study. Neurology 78(24):1939–1945

    Article  CAS  PubMed  Google Scholar 

  42. Wang JJ, Lin WY, Lu CS et al (2011) Parkinson disease: diagnostic utility of diffusion kurtosis imaging. Radiology 261(1):210–217

    Article  PubMed  Google Scholar 

  43. Stoessl AJ, Lehericy S, Strafella AP (2014) Imaging insights into basal ganglia function, Parkinson’s disease, and dystonia. Lancet 384:532–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Schwarz ST, Abaei M, Gontu V et al (2013) Diffusion tensor imaging of nigral degeneration in Parkinson’s disease: a region-of-interest and voxel-based study at 3 T and systematic review with meta-analysis. Neuroimage Clin 3:481–488

    Article  PubMed  PubMed Central  Google Scholar 

  45. Menke RA, Szewczyk-Krolikowski K, Jbabdi S et al (2014) Comprehensive morphometry of subcortical grey matter structures in early-stage Parkinson’s disease. Hum Brain Mapp 35:1681–1690

    Article  PubMed  Google Scholar 

  46. Ziegler E, Rouillard M, Andre E et al (2014) Mapping track density changes in nigrostriatal and extranigral pathways in Parkinson’s disease. Neuroimage 99:498–508

    Article  PubMed  PubMed Central  Google Scholar 

  47. Nemmi F, Sabatini U, Rascol O et al (2015) Parkinson’s disease and local atrophy in subcortical nuclei: insight from shape analysis. Neurobiol Aging 36:424–433

    Article  PubMed  Google Scholar 

  48. Tessa C, Giannelli M, Della Nave R et al (2008) A whole-brain analysis in de novo Parkinson disease. Am J Neuroradiol 29:674–680

    Article  CAS  PubMed  Google Scholar 

  49. Nobili F, Arnaldi D, Campus C et al (2011) Brain perfusion correlates of cognitive and nigrostriatal functions in de novo Parkinson’s disease. Eur J Nucl Med Mol Imaging 38:2209–2218

    Article  PubMed  Google Scholar 

  50. Planetta PJ, Schulze ET, Geary EK et al (2013) Thalamic projection fiber integrity in de novo Parkinson disease. Am J Neuroradiol 34:74–79

    Article  CAS  PubMed  Google Scholar 

  51. Lee HM, Kwon KY, Kim MJ et al (2014) Subcortical grey matter changes in untreated, early stage Parkinson’s disease without dementia. Parkinsonism Relat Disord 20:622–626

    Article  PubMed  Google Scholar 

  52. Luo C, Song W, Chen Q et al (2014) Reduced functional connectivity in early-stage drug-naive Parkinson’s disease: a resting-state fMRI study. Neurobiol Aging 35:431–441

    Article  PubMed  Google Scholar 

  53. Tessa C, Lucetti C, Giannelli M et al (2014) Progression of brain atrophy in the early stages of Parkinson’s disease: a longitudinal tensor-based morphometry study in de novo patients without cognitive impairment. Hum Brain Mapp 35:3932–3944

    Article  PubMed  Google Scholar 

  54. Vriend C, Gerrits NJ, Berendse HW et al (2015) Failure of stop and go in de novo Parkinson’s disease—a functional magnetic resonance imaging study. Neurobiol Aging 36:470–475

    Article  PubMed  Google Scholar 

  55. Caligiuri ME, Nisticò R, Arabia G et al (2016) Alterations of putaminal shape in de novo Parkinson’s disease. Mov Disord. doi:10.1002/mds.26550

    PubMed  Google Scholar 

  56. Sharman M, Valabregue R, Perlbarg V et al (2013) Parkinson’s disease patients show reduced cortical-subcortical sensorimotor connectivity. Mov Disord 28:447–454

    Article  CAS  PubMed  Google Scholar 

  57. Burton EJ, McKeith IG, Burn DJ et al (2004) Cerebral atrophy in Parkinson’s disease with and without dementia: a comparison with Alzheimer’s disease, dementia with Lewy bodies and controls. Brain 127:791–800

    Article  PubMed  Google Scholar 

  58. Summerfield C, Junque C, Tolosa E et al (2005) Structural brain changes in Parkinson disease with dementia: a voxel-based morphometry study. Arch Neurol 62:281–285

    Article  PubMed  Google Scholar 

  59. Jahanshahi M, Jenkins IH, Brown RG et al (1995) Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 118(4):913–933

    Article  PubMed  Google Scholar 

  60. Playford ED, Jenkins IH, Passingham RE et al (1992) DJ impaired mesial frontal and putamen activation in Parkinson’s disease: a positron emission tomography study. Ann Neurol 32:151–161

    Article  CAS  PubMed  Google Scholar 

  61. Rascol O, Sabatini U, Chollet F et al (1992) Supplementary and primary sensory motor area activity in Parkinson’s disease. Regional cerebral blood flow changes during finger movements and effects of apomorphine. Arch Neurol 49:144–148

    Article  CAS  PubMed  Google Scholar 

  62. Rascol O, Sabatini U, Chollet F et al (1994) Normal activation of the supplementary motor area in patients with Parkinson’s disease undergoing long-term treatment with levodopa. J Neurol Neurosurg Psychiatry 57:567–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Samuel M, Ceballos-Baumann AO, Boecker H, Brooks DJ (2001) Motor imagery in normal subjects and Parkinson’s disease patients: an H215O PET study. Neuroreport 12:821–828

    Article  CAS  PubMed  Google Scholar 

  64. Sabatini U, Boulanouar K, Fabre N et al (2000) Cortical motor reorganization in akinetic patients with Parkinson’s disease: a functional MRI study. Brain 123(2):394–403

    Article  PubMed  Google Scholar 

  65. Haslinger B, Erhard P, Kampfe N et al (2001) Event-related functional magnetic resonance imaging in Parkinson’s disease before and after levodopa. Brain 124:558–570

    Article  CAS  PubMed  Google Scholar 

  66. Nicoletti G, Lodi R, Condino F et al (2006) Apparent diffusion coefficient measurements of the middle cerebellar peduncle differentiate the Parkinson variant of MSA from Parkinson’s disease and progressive supranuclear palsy. Brain 129(Pt 10):2679–2687

    Article  PubMed  Google Scholar 

  67. Cherubini A, Morelli M, Nisticò R et al (2013) Magnetic resonance support vector machine discriminates between Parkinson disease and progressive supranuclear palsy. Mov Disord 29(2):266–269

    Article  PubMed  Google Scholar 

  68. Wang PS, Wu HM, Lin CP et al (2011) Use of diffusion tensor imaging to identify similarities and differences between cerebellar and Parkinsonism forms of multiple system atrophy. Neuroradiology 53(7):471–481

    Article  PubMed  Google Scholar 

  69. Boelmans K, Bodammer NC, Suchorska B et al (2010) Diffusion tensor imaging of the corpus callosum differentiates corticobasal syndrome from Parkinson’s disease. Parkinsonism Relat Disord 16(8):498–502

    Article  PubMed  Google Scholar 

  70. Cherubini A, Nisticò R, Novellino F et al (2014) Magnetic resonance support vector machine discriminates essential tremor with rest tremor from tremor-dominant Parkinson disease. Mov Disord 29(9):1216–1219

    Article  PubMed  Google Scholar 

  71. Prodoehl J, Li H, Planetta PJ et al (2013) Diffusion tensor imaging of Parkinson’s disease, atypical parkinsonism, and essential tremor. Mov Disord 28(13):1816–1822

    Article  PubMed  Google Scholar 

  72. Nair SR, Tan LK, Mohd Ramli N et al (2013) A decision tree for differentiating multiple system atrophy from Parkinson’s disease using 3-T MR imaging. Eur Radiol 23(6):1459–1466

    Article  PubMed  Google Scholar 

  73. Hacker CD, Perlmutter JS, Criswell SR et al (2012) Resting state functional connectivity of the striatum in Parkinson’s disease. Brain 135(12):3699–3711

    Article  PubMed  PubMed Central  Google Scholar 

  74. Helmich RC, Derikx LC, Bakker M et al (2010) Spatial remapping of cortico-striatal connectivity in Parkinson’s disease. Cereb Cortex 20(5):1175–1186

    Article  PubMed  Google Scholar 

  75. Cerasa A, Koch G, Donzuso G et al (2015) A network centred on the inferior frontal cortex is critically involved in levodopa-induced dyskinesias. Brain 138(2):414–427

    Article  PubMed  Google Scholar 

  76. Hagmann P (2005) From diffusion MRI to brain connectomics. Signal Processing Institute. Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, pp. 127

    Google Scholar 

  77. Sporns O, Tononi G, Kotter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1:e42

    Article  PubMed  PubMed Central  Google Scholar 

  78. Skidmore F, Korenkevych D, Liu Y et al (2011) Connectivity brain networks based on wavelet correlation analysis in Parkinson fMRI data. Neurosci Lett 499:47–51

    Article  CAS  PubMed  Google Scholar 

  79. Wei L, Zhang J, Long Z et al (2014) Reduced topological efficiency in cortical-basal ganglia motor network of Parkinson’s disease: a resting state fMRI study. PLoS One 9:e108124

    Article  PubMed  PubMed Central  Google Scholar 

  80. Pereira JB, Aarsland D, Ginestet CE et al (2015) Aberrant cerebral network topology and mild cognitive impairment in early Parkinson’s disease. Hum Brain Mapp 36:2980–2995

    Article  PubMed  Google Scholar 

  81. Biomedical FAST (2001) NIH definition of biomarker. Clin Pharmacol Ther 69:89–95

    Article  Google Scholar 

  82. Gutman S, Kessler LG (2006) The US food and drug administration perspective on cancer biomarker development. Nat Rev Cancer 6(7):565–571

    Article  CAS  PubMed  Google Scholar 

  83. Marek K, Jennings D, Lasch S et al (2011) The Parkinson Progression Marker Initiative (PPMI). Prog Neurobiol 95(4):629–635

    Article  Google Scholar 

  84. Ofori E, Du G, Babcock D et al (2016) Parkinson’s disease biomarkers program brain imaging repository. Neuroimage 124:1120–1124

    Article  PubMed  Google Scholar 

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Correspondence to Umberto Sabatini .

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Cherubini, A., Caligiuri, M.E., Péran, P., Sabatini, U. (2017). High-Field Neuroimaging in Parkinson’s Disease. In: Scarabino, T., Pollice, S., Popolizio, T. (eds) High Field Brain MRI. Springer, Cham. https://doi.org/10.1007/978-3-319-44174-0_17

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