PET and SPECT Imaging in Parkinsonian Syndromes

  • Chris C. Tang
  • Martin Niethammer
  • Patricia J. Allen
  • Klaus (Nico) L. Leenders
  • David Eidelberg
Chapter

Abstract

Parkinson’s disease and parkinsonian disorders can present with a variety of symptoms, and there is often significant overlap between the different disorders. Diagnosis typically relies on clinical examination, especially at follow-up visits, which has limitations. Neuroimaging has played a major role in the elucidation of anatomical and functional abnormalities in different parkinsonian disorders. Various imaging techniques have been investigated for their potential to aid in diagnosis during routine clinical practice. In this chapter, we describe the use of functional imaging with PET and SPECT in the research of parkinsonian syndromes, including multiple system atrophy (MSA), progressive supranuclear palsy (PSP), and corticobasal degeneration (CBD). We focus on the utility of these imaging techniques to facilitate differential diagnosis and assess disease progression in patients, especially in the early stages of disease.

Keywords

Positron Emission Tomography Multiple System Atrophy Dementia With Lewy Body Progressive Supranuclear Palsy Parkinsonian Syndrome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

[11C](R)-PK11195

11C(R)-1-(2-chlorophenyl)-N-methyl-N-(1-methylpropyl)-3-isoquinolinecarboxamide

APS

Atypical parkinsonian syndromes

CBD

Corticobasal degeneration

CIT

Carboxymethyoxy-3-β-(4-iodophenyl) tropane

COX-2

Cyclooxygenase-2

CVLT

California Verbal Learning Test

DAT

Dopamine transporter

DWI

Diffusion-weighted imaging

FDG

18F-fluorodeoxyglucose

FP

Fluoropropyl

HVLT

Hooper Verbal Learning Test

123I-IBF

123I-Iodolisuride

123I-IBZM

123I-Iodobenzamide

DLB

Dementia with Lewy bodies

LN

Lentiform nucleus

MCI

Mild cognitive impairment

MIBG

Meta-123I-iodobenzylguanidine

MR

Magnetic resonance

MRI

Magnetic resonance imaging

MSA

Multiple system atrophy

MSARP

Multiple system atrophy-related pattern

MSA-C

Multiple system atrophy-cerebellar

MSA-P

Multiple system atrophy-parkinsonian

PBBS

Peripheral benzodiazepine binding site

PCA

Principal component analysis

PAGF

Pure akinesia with gait freezing

PD

Parkinson’s disease

PDCP

Parkinson’s disease-related cognitive pattern

PET

Positron emission tomography

PDRP

Parkinson’s disease-related motor pattern

PMC

Premotor cortex

Pre-SMA

Pre-supplementary motor area

PSP

Progressive supranuclear palsy

PSPRP

Progressive supranuclear palsy-related pattern

SMA

Supplementary motor area

SN

Substantia nigra

SPM

Spatial parametric mapping

SPECT

Single-photon emission computed tomography

TCS

Transcranial sonography

TSPO

Translocator protein 18 kDa

99mTc-ECD

Technetium-99m ethyl cysteinate dimer

Notes

Acknowledgments

This work was supported by the National Institutes of Health [NINDS R01 NS 35069 and P50 NS 38370 to D.E.], the General Clinical Research Center of the Feinstein Institute for Medical Research, North Shore-LIJ Health System [National Center for Research Resources (NCRR), a component of the National Institutes of Health, M01 RR018535], and the International Parkinson Fonds, Hoofddorp, the Netherlands.

References

  1. Abe K, Takanashi M, Yanagihara T (2000) Fatigue in patients with Parkinson’s disease. Behav Neurol 12:103–106PubMedCrossRefGoogle Scholar
  2. Bartels AL, Leenders KL (2007) Neuroinflammation in the pathophysiology of Parkinson’s disease: evidence from animal models to human in vivo studies with [11C]-PK11195 PET. Mov Disord 22:1852–1856PubMedCrossRefGoogle Scholar
  3. Bartels AL, de Jong BM, Giladi N, Schaafsma JD, Maguire RP, Veenma L, Pruim J, Balash Y, Youdim MB, Leenders KL (2006) Striatal dopa and glucose metabolism in PD patients with freezing of gait. Mov Disord 21:1326–1332PubMedCrossRefGoogle Scholar
  4. Bartels AL, Willemsen AT, Doorduin J, de Vries EF, Dierckx RA, Leenders KL (2010) [11C]-PK11195 PET: quantification of neuroinflammation and a monitor of anti-inflammatory treatment in Parkinson’s disease? Parkinsonism Relat Disord 16:57–59PubMedCrossRefGoogle Scholar
  5. Becker G, Seufert J, Bogdahn U, Reichmann H, Reiners K (1995) Degeneration of substantia nigra in chronic Parkinson’s disease visualized by transcranial color-coded real-time sonography. Neurology 45:182–184PubMedCrossRefGoogle Scholar
  6. Benamer H, Grosset D (2009) Vascular parkinsonism: a clinical review. Eur Neurol 61:11–15PubMedCrossRefGoogle Scholar
  7. Benamer HT, Patterson J, Wyper DJ, Hadley DM, Macphee GJ, Grosset DG (2000) Correlation of Parkinson’s disease severity and duration with 123I-FP-CIT SPECT striatal uptake. Mov Disord 15:692–698PubMedCrossRefGoogle Scholar
  8. Benamer HT, Oertel WH, Patterson J, Hadley DM, Pogarell O, Hoffken H, Gerstner A, Grosset DG (2003) Prospective study of presynaptic dopaminergic imaging in patients with mild parkinsonism and tremor disorders: part 1. Baseline and 3-month observations. Mov Disord 18:977–984PubMedCrossRefGoogle Scholar
  9. Berg D, Siefker C, Becker G (2001) Echogenicity of the substantia nigra in Parkinson’s disease and its relation to clinical findings. J Neurol 248:684–689PubMedCrossRefGoogle Scholar
  10. Booij J, Tissingh G, Boer GJ, Speelman JD, Stoof JC, Janssen AG, Wolters EC, van Royen EA (1997) [123I]FP-CIT SPECT shows a pronounced decline of striatal dopamine transporter labelling in early and advanced Parkinson’s disease. J Neurol Neurosurg Psychiatry 62:133–140PubMedCentralPubMedCrossRefGoogle Scholar
  11. Bosman T, Van Laere K, Santens P (2003) Anatomically standardised 99mTc-ECD brain perfusion SPEt allows accurate differentiation between healthy volunteers, multiple system atrophy and idiopathic Parkinson’s disease. Eur J Nucl Med Mol Imaging 30:16–24Google Scholar
  12. Cicchetti F, Brownell AL, Williams K, Chen YI, Livni E, Isacson O (2002) Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging. Eur J Neurosci 15:991–998PubMedCrossRefGoogle Scholar
  13. Cordato N, Pantelis C, Halliday G, Velakoulis D, Wood S, Stuart G, Currie J, Soo M, Olivieri G, Broe G, Morris J (2002) Frontal atrophy correlates with behavioural changes in progressive supranuclear palsy. Brain 125:789–800PubMedCrossRefGoogle Scholar
  14. Davie C, Wenning G, Barker G, Tofts P, Kendall B, Quinn N, McDonald W, Marsden C, Miller D (1995) Differentiation of multiple system atrophy from idiopathic Parkinson’s disease using proton magnetic resonance spectroscopy. Ann Neurol 37:204–210PubMedCrossRefGoogle Scholar
  15. Dodel R, Spottke A, Gerhard A, Reuss A, Reinecker S, Schimke N, Trenkwalder C, Sixel-Doring F, Herting B, Kamm C, Gasser T, Sawires M, Geser F, Kollensperger M, Seppi K, Kloss M, Krause M, Daniels C, Deuschl G, Bottger S, Naumann M, Lipp A, Gruber D, Kupsch A, Du Y, Turkheimer F, Brooks DJ, Klockgether T, Poewe W, Wenning G, Schade-Brittinger C, Oertel WH, Eggert K (2010) Minocycline 1-year therapy in multiple-system-atrophy: effect on clinical symptoms and [(11)C] (R)-PK11195 PET (MEMSA-trial). Mov Disord 25:97–107PubMedCrossRefGoogle Scholar
  16. Eckert T, Eidelberg D (2005) Neuroimaging and therapeutics in movement disorders. NeuroRx 2:361–371PubMedCentralPubMedCrossRefGoogle Scholar
  17. Eckert T, Barnes A, Dhawan V, Frucht S, Gordon MF, Feigin AS, Eidelberg D (2005) FDG PET in the differential diagnosis of parkinsonian disorders. Neuroimage 26:912–921PubMedCrossRefGoogle Scholar
  18. Eckert T, Van Laere K, Tang C, Lewis DE, Edwards C, Santens P, Eidelberg D (2007) Quantification of Parkinson’s disease-related network expression with ECD SPECT. Eur J Nucl Med Mol Imaging 34:496–501PubMedCrossRefGoogle Scholar
  19. Eckert T, Tang C, Ma Y, Brown N, Lin T, Frucht S, Feigin A, Eidelberg D (2008) Abnormal metabolic networks in atypical parkinsonism. Mov Disord 23:727–733PubMedCrossRefGoogle Scholar
  20. Eidelberg D (2009) Metabolic brain networks in neurodegenerative disorders: a functional imaging approach. Trends Neurosci 32:548–557PubMedCentralPubMedCrossRefGoogle Scholar
  21. Eidelberg D, Takikawa S, Moeller JR, Dhawan V, Redington K, Chaly T, Robeson W, Dahl JR, Margouleff D, Fazzini E et al (1993) Striatal hypometabolism distinguishes nigrostriatal degeneration from Parkinson’s disease. Ann Neurol 33:518–527PubMedCrossRefGoogle Scholar
  22. Eidelberg D, Moeller J, Dhawan V, Spetsieris P, Takikawa S, Ishikawa T, Chaly T, Robeson W, Margouleff D, Przedborski S et al (1994) The metabolic topography of parkinsonism. J Cereb Blood Flow Metab 14:783–801PubMedCrossRefGoogle Scholar
  23. El Fakhri G, Habert MO, Maksud P, Kas A, Malek Z, Kijewski MF, Lacomblez L (2006) Quantitative simultaneous (99m)Tc-ECD/123I-FP-CIT SPECT in Parkinson’s disease and multiple system atrophy. Eur J Nucl Med Mol Imaging 33:87–92PubMedCrossRefGoogle Scholar
  24. Eshuis SA, Maguire RP, Leenders KL, Jonkman S, Jager PL (2006) Comparison of FP-CIT SPECT with F-DOPA PET in patients with de novo and advanced Parkinson’s disease. Eur J Nucl Med Mol Imaging 33:200–209PubMedCrossRefGoogle Scholar
  25. Eshuis SA, Jager PL, Maguire RP, Jonkman S, Dierckx RA, Leenders KL (2009) Direct comparison of FP-CIT SPECT and F-DOPA PET in patients with Parkinson’s disease and healthy controls. Eur J Nucl Med Mol Imaging 36:454–462PubMedCrossRefGoogle Scholar
  26. Federico F, Simone I, Lucivero V, Iliceto G, De Mari M, Giannini P, Mezzapesa D, Tarantino A, Lamberti P (1997) Proton magnetic resonance spectroscopy in Parkinson’s disease and atypical parkinsonian disorders. Mov Disord 12:903–909PubMedCrossRefGoogle Scholar
  27. Feigin A, Tang C, Ma Y, Mattis P, Zgaljardic D, Guttman M, Paulsen J, Dhawan V, Eidelberg D (2007) Thalamic metabolism and symptom onset in preclinical Huntington’s disease. Brain 130:2858–2867PubMedCrossRefGoogle Scholar
  28. Gaenslen A, Gasser T, Berg D (2008) Nutrition and the risk for Parkinson’s disease: review of the literature. J Neural Transm 115:703–713PubMedCrossRefGoogle Scholar
  29. Gerhard A, Banati RB, Goerres GB, Cagnin A, Myers R, Gunn RN, Turkheimer F, Good CD, Mathias CJ, Quinn N, Schwarz J, Brooks DJ (2003) [11C](R)-PK11195 PET imaging of microglial activation in multiple system atrophy. Neurology 61:686–689PubMedCrossRefGoogle Scholar
  30. Gerhard A, Watts J, Trender-Gerhard I, Turkheimer F, Banati RB, Bhatia K, Brooks DJ (2004) In vivo imaging of microglial activation with [11C](R)-PK11195 PET in corticobasal degeneration. Mov Disord 19:1221–1226PubMedCrossRefGoogle Scholar
  31. Gerhard A, Pavese N, Hotton G, Turkheimer F, Es M, Hammers A, Eggert K, Oertel W, Banati RB, Brooks DJ (2006a) In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson’s disease. Neurobiol Dis 21:404–412PubMedCrossRefGoogle Scholar
  32. Gerhard A, Trender-Gerhard I, Turkheimer F, Quinn NP, Bhatia KP, Brooks DJ (2006b) In vivo imaging of microglial activation with [11C](R)-PK11195 PET in progressive supranuclear palsy. Mov Disord 21:89–93PubMedCrossRefGoogle Scholar
  33. Ghaemi M, Hilker R, Rudolf J, Sobesky J, Heiss WD (2002) Differentiating multiple system atrophy from Parkinson’s disease: contribution of striatal and midbrain MRI volumetry and multi-tracer PET imaging. J Neurol Neurosurg Psychiatry 73:517–523PubMedCentralPubMedCrossRefGoogle Scholar
  34. Gilman S, Wenning G, Low P, Brooks D, Mathias C, Trojanowski J, Wood N, Colosimo C, Durr A, Fowler C, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676PubMedCentralPubMedCrossRefGoogle Scholar
  35. Habeck C, Foster N, Perneczky R, Kurz A, Alexopoulos P, Koeppe R, Drzezga A, Stern Y (2008) Multivariate and univariate neuroimaging biomarkers of Alzheimer’s disease. Neuroimage 40:1503–1515PubMedCentralPubMedCrossRefGoogle Scholar
  36. Henkel K, Karitzky J, Schmid M, Mader I, Glatting G, Unger JW, Neumaier B, Ludolph AC, Reske SN, Landwehrmeyer GB (2004) Imaging of activated microglia with PET and [11C]PK 11195 in corticobasal degeneration. Mov Disord 19:817–821Google Scholar
  37. Huang C, Mattis P, Tang C, Perrine K, Carbon M, Eidelberg D (2007) Metabolic brain networks associated with cognitive function in Parkinson’s disease. Neuroimage 34:714–723PubMedCrossRefGoogle Scholar
  38. Huang C, Mattis P, Perrine K, Brown N, Dhawan V, Eidelberg D (2008) Metabolic abnormalities associated with mild cognitive impairment in Parkinson disease. Neurology 70:1470–1477PubMedCrossRefGoogle Scholar
  39. Hughes A, Daniel S, Kilford L, Lees A (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184PubMedCentralPubMedCrossRefGoogle Scholar
  40. Hughes A, Daniel S, Ben-Shlomo Y, Lees A (2002) The accuracy of diagnosis of parkinsonian syndromes in a specialist movement disorder service. Brain 125:861–870PubMedCrossRefGoogle Scholar
  41. Ichise M, Kim YJ, Ballinger JR, Vines D, Erami SS, Tanaka F, Lang AE (1999) SPECT imaging of pre- and postsynaptic dopaminergic alterations in L-dopa-untreated PD. Neurology 52:1206–1214PubMedCrossRefGoogle Scholar
  42. Imamura K, Hishikawa N, Sawada M, Nagatsu T, Yoshida M, Hashizume Y (2003) Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson’s disease brains. Acta Neuropathol 106:518–526PubMedCrossRefGoogle Scholar
  43. Ishizawa K, Dickson DW (2001) Microglial activation parallels system degeneration in progressive supranuclear palsy and corticobasal degeneration. J Neurol Exp Neurol 60:647–657Google Scholar
  44. Ishizawa K, Komori T, Sasaki S, Arai N, Mizutani T, Hirose T (2004) Microglial activation parallels system degeneration in multiple system atrophy. J Neurol Exp Neurol 63:43–52Google Scholar
  45. Josephs K, Dickson D (2003) Diagnostic accuracy of progressive supranuclear palsy in the society for progressive supranuclear palsy brain bank. Mov Disord 18:1018–1026PubMedCrossRefGoogle Scholar
  46. Kaasinen V, Ruottinen HM, Nagren K, Lehikoinen P, Oikonen V, Rinne JO (2000) Upregulation of putaminal dopamine D2 receptors in early Parkinson’s disease: a comparative PET study with [11C] raclopride and [11C]N-methylspiperone. J Nucl Med 41:65–70PubMedGoogle Scholar
  47. Kanazawa M, Shimohata T, Terajima K, Onodera O, Tanaka K, Tsuji S, Okamoto K, Nishizawa M (2004) Quantitative evaluation of brainstem involvement in multiple system atrophy by diffusion-weighted MR imaging. J Neurol 251:1121–1124PubMedGoogle Scholar
  48. Kim YJ, Ichise M, Ballinger JR, Vines D, Erami SS, Tatschida T, Lang AE (2002) Combination of dopamine transporter and D2 receptor SPECT in the diagnostic evaluation of PD, MSA, and PSP. Mov Disord 17:303–312PubMedCrossRefGoogle Scholar
  49. Klaffke S, Kuhn AA, Plotkin M, Amthauer H, Harnack D, Felix R, Kupsch A (2006) Dopamine transporters, D2 receptors, and glucose metabolism in corticobasal degeneration. Mov Disord 21:1724–1727PubMedCrossRefGoogle Scholar
  50. Klein RC, de Jong BM, de Vries JJ, Leenders KL (2005) Direct comparison between regional cerebral metabolism in progressive supranuclear palsy and Parkinson’s disease. Mov Disord 20:1021–1030PubMedCrossRefGoogle Scholar
  51. Knudsen GM, Karlsborg M, Thomsen G, Krabbe K, Regeur L, Nygaard T, Videbaek C, Werdelin L (2004) Imaging of dopamine transporters and D2 receptors in patients with Parkinson’s disease and multiple system atrophy. Eur J Nucl Med Mol Imaging 31:1631–1638PubMedCrossRefGoogle Scholar
  52. Leenders KL (2003) Significance of non-presynaptic SPECT tracer methods in Parkinson’s disease. Mov Disord 18(Suppl 7):S39–S42PubMedCrossRefGoogle Scholar
  53. Linder J, Birgander R, Olsson I, Riklund K, Larsson A, Edstrom M, Stenlund H, Forsgren L (2009) Degenerative changes were common in brain magnetic resonance imaging in patients with newly diagnosed Parkinson’s disease in a population-based cohort. J Neurol 256:1671–1680PubMedCrossRefGoogle Scholar
  54. Litvan I (2003) Update on epidemiological aspects of progressive supranuclear palsy. Mov Disord 18(Suppl 6):S43–S50PubMedCrossRefGoogle Scholar
  55. Litvan I, Goetz CG, Jankovic J, Wenning GK, Booth V, Bartko JJ, McKee A, Jellinger K, Lai EC, Brandel JP, Verny M, Chaudhuri KR, Pearce RK, Agid Y (1997) What is the accuracy of the clinical diagnosis of multiple system atrophy? A clinicopathologic study. Arch Neurol 54:937–944PubMedCrossRefGoogle Scholar
  56. Ma Y, Tang C, Spetsieris PG, Dhawan V, Eidelberg D (2007) Abnormal metabolic network activity in Parkinson’s disease: test-retest reproducibility. J Cereb Blood Flow Metab 27:597–605PubMedCrossRefGoogle Scholar
  57. Marek KL, Seibyl JP, Zoghbi SS, Zea-Ponce Y, Baldwin RM, Fussell B, Charney DS, van Dyck C, Hoffer PB, Innis RP (1996) [123I] beta-CIT/SPECT imaging demonstrates bilateral loss of dopamine transporters in hemi-Parkinson’s disease. Neurology 46:231–237PubMedCrossRefGoogle Scholar
  58. Marek K, Innis R, van Dyck C, Fussell B, Early M, Eberly S, Oakes D, Seibyl J (2001) [123I]beta-CIT SPECT imaging assessment of the rate of Parkinson’s disease progression. Neurology 57:2089–2094PubMedCrossRefGoogle Scholar
  59. Marshall VL, Reininger CB, Marquardt M, Patterson J, Hadley DM, Oertel WH, Benamer HT, Kemp P, Burn D, Tolosa E, Kulisevsky J, Cunha L, Costa D, Booij J, Tatsch K, Chaudhuri KR, Ulm G, Pogarell O, Hoffken H, Gerstner A, Grosset DG (2009) Parkinson’s disease is overdiagnosed clinically at baseline in diagnostically uncertain cases: a 3-year European multicenter study with repeat [123I]FP-CIT SPECT. Mov Disord 24:500–508PubMedCrossRefGoogle Scholar
  60. Minnerop M, Specht K, Ruhlmann J, Schimke N, Abele M, Weyer A, Wullner U, Klockgether T (2007) Voxel-based morphometry and voxel-based relaxometry in multiple system atrophy-a comparison between clinical subtypes and correlations with clinical parameters. Neuroimage 36:1086–1095PubMedCrossRefGoogle Scholar
  61. Nicoletti G, Lodi R, Condino F, Tonon C, Fera F, Malucelli E, Manners D, Zappia M, Morgante L, Barone P, Barbiroli B, Quattrone A (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 129:2679–2687PubMedCrossRefGoogle Scholar
  62. Nurmi E, Ruottinen HM, Kaasinen V, Bergman J, Haaparanta M, Solin O, Rinne JO (2000) Progression in Parkinson’s disease: a positron emission tomography study with a dopamine transporter ligand [18F]CFT. Ann Neurol 47:804–808PubMedCrossRefGoogle Scholar
  63. Ouchi Y, Yoshikawa E, Sekine Y, Futatsubashi M, Kanno T, Ogusu T, Torizuka T (2005) Microglial activation and dopamine terminal loss in early Parkinson’s disease. Ann Neurol 57:168–175PubMedCrossRefGoogle Scholar
  64. Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapere JJ, Lindemann P, Norenberg MD, Nutt D, Weizman A, Zhang MR, Gavish M (2006) Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 27:402–409PubMedCrossRefGoogle Scholar
  65. Papp M, Kahn J, Lantos P (1989) Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (nigrostriatal degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 94:79–100PubMedCrossRefGoogle Scholar
  66. Park HK, Kim JS, Im KC, Oh SJ, Kim MJ, Lee JH, Chung SJ, Lee MC (2009) Functional brain imaging in pure akinesia with gait freezing: [18F] FDG PET and [18F] FP-CIT PET analyses. Mov Disord 24:237–245PubMedCrossRefGoogle Scholar
  67. Paviour D, Price S, Stevens J, Lees A, Fox N (2005) Quantitative MRI measurement of superior cerebellar peduncle in progressive supranuclear palsy. Neurology 64:675–679PubMedCrossRefGoogle Scholar
  68. Perju-Dumbrava LD, Kovacs GG, Pirker S, Jellinger K, Hoffmann M, Asenbaum S, Pirker W (2012) Dopamine transporter imaging in autopsy-confirmed Parkinson’s disease and multiple system atrophy. Mov Disord 27:65–71PubMedCrossRefGoogle Scholar
  69. Pirker W, Asenbaum S, Bencsits G, Prayer D, Gerschlager W, Deecke L, Brucke T (2000) [123I]beta-CIT SPECT in multiple system atrophy, progressive supranuclear palsy, and corticobasal degeneration. Mov Disord 15:1158–1167PubMedCrossRefGoogle Scholar
  70. Pirker W, Djamshidian S, Asenbaum S, Gerschlager W, Tribl G, Hoffmann M, Brucke T (2002) Progression of dopaminergic degeneration in Parkinson’s disease and atypical parkinsonism: a longitudinal beta-CIT SPECT study. Mov Disord 17:45–53PubMedCrossRefGoogle Scholar
  71. Plotkin M, Amthauer H, Klaffke S, Kuhn A, Ludemann L, Arnold G, Wernecke KD, Kupsch A, Felix R, Venz S (2005) Combined 123I-FP-CIT and 123I-IBZM SPECT for the diagnosis of parkinsonian syndromes: study on 72 patients. J Neural Transm 112:677–692PubMedCrossRefGoogle Scholar
  72. Poston KL, Eidelberg D (2009) Network biomarkers for the diagnosis and treatment of movement disorders. Neurobiol Dis 35:141–147PubMedCrossRefGoogle Scholar
  73. Poston K, Tang C, Eckert T, Dhawan V, Frucht S, Vonsattel J, Fahn S, Eidelberg D (2012) Network correlates of disease severity in multiple system atrophy. Neurology 78:1237–1244PubMedCentralPubMedCrossRefGoogle Scholar
  74. Scherfler C, Seppi K, Donnemiller E, Goebel G, Brenneis C, Virgolini I, Wenning GK, Poewe W (2005) Voxel-wise analysis of [123I]beta-CIT SPECT differentiates the Parkinson variant of multiple system atrophy from idiopathic Parkinson’s disease. Brain 128:1605–1612PubMedCrossRefGoogle Scholar
  75. Schott J, Williams D, Butterworth R, Janssen J, Larner A, Holton J, Rossor M (2007) Shunt responsive progressive supranuclear palsy? Mov Disord 22:902–903PubMedCrossRefGoogle Scholar
  76. Seibyl JP, Marek KL, Quinlan D, Sheff K, Zoghbi S, Zea-Ponce Y, Baldwin RM, Fussell B, Smith EO, Charney DS, van Dyck C et al (1995) Decreased single-photon emission computed tomographic [123I]beta-CIT striatal uptake correlates with symptom severity in Parkinson’s disease. Ann Neurol 38:589–598PubMedCrossRefGoogle Scholar
  77. Seppi K, Schocke M (2005) An update on conventional and advanced magnetic resonance imaging techniques in the differential diagnosis of neurodegenerative parkinsonism. Curr Opin Neurol 18:370–375PubMedCrossRefGoogle Scholar
  78. Soliveri P, Monza D, Paridi D, Radice D, Grisoli M, Testa D, Savoiardo M, Girotti F (1999) Cognitive and magnetic resonance imaging aspects of corticobasal degeneration and progressive supranuclear palsy. Neurology 53:502–507PubMedCrossRefGoogle Scholar
  79. Spetsieris P, Ma Y, Dhawan V, Eidelberg D (2009) Differential diagnosis of parkinsonian syndromes using PCA-based functional imaging features. Neuroimage 45:1241–1252PubMedCrossRefGoogle Scholar
  80. Spiegel J, Mollers MO, Jost WH, Fuss G, Samnick S, Dillmann U, Becker G, Kirsch CM (2005) FP-CIT and MIBG scintigraphy in early Parkinson’s disease. Mov Disord 20:552–561PubMedCrossRefGoogle Scholar
  81. Staffen W, Mair A, Unterrainer J, Trinka E, Ladurner G (2000) Measuring the progression of idiopathic Parkinson’s disease with [123I] beta-CIT SPECT. J Neural Transm 107:543–552PubMedCrossRefGoogle Scholar
  82. Sudmeyer M, Antke C, Zizek T, Beu M, Nikolaus S, Wojtecki L, Schnitzler A, Muller HW (2011) Diagnostic accuracy of combined FP-CIT, IBZM, and MIBG scintigraphy in the differential diagnosis of degenerative parkinsonism: a multidimensional statistical approach. J Nucl Med 52:733–740PubMedCrossRefGoogle Scholar
  83. Tang C, Poston K, Dhawan V, Eidelberg D (2010a) Abnormalities in metabolic network activity precede the onset of motor symptoms in Parkinson’s disease. J Neurosci 30:1049–1056PubMedCentralPubMedCrossRefGoogle Scholar
  84. Tang C, Poston K, Eckert T, Feigin A, Frucht S, Gudesblatt M, Dhawan V, Lesser M, Vonsattel J, Fahn S, Eidelberg D (2010b) Differential diagnosis of parkinsonism: a metabolic imaging study using pattern analysis. Lancet Neurol 9:149–158PubMedCrossRefGoogle Scholar
  85. Teune LK, Bartels AL, de Jong BM, Willemsen AT, Eshuis SA, de Vries JJ, van Oostrom JC, Leenders KL (2010) Typical cerebral metabolic patterns in neurodegenerative brain diseases. Mov Disord 25:2395–2404PubMedCrossRefGoogle Scholar
  86. Teune LK, Renken RJ, Mudali D, De Jong BM, Dierckx RA, Roerdink JB, Leenders KL (2013) Validation of parkinsonian disease-related metabolic brain patterns. Mov Disord 28:547–551PubMedCrossRefGoogle Scholar
  87. Van Laere K, Casteels C, De Ceuninck L, Vanbilloen B, Maes A, Mortelmans L, Vandenberghe W, Verbruggen A, Dom R (2006) Dual-tracer dopamine transporter and perfusion SPECT in differential diagnosis of parkinsonism using template-based discriminant analysis. J Nucl Med 47:384–392PubMedGoogle Scholar
  88. Varrone A, Marek KL, Jennings D, Innis RB, Seibyl JP (2001) [(123)I]beta-CIT SPECT imaging demonstrates reduced density of striatal dopamine transporters in Parkinson’s disease and multiple system atrophy. Mov Disord 16:1023–1032PubMedCrossRefGoogle Scholar
  89. Vlaar AM, de Nijs T, Kessels AG, Vreeling FW, Winogrodzka A, Mess WH, Tromp SC, van Kroonenburgh MJ, Weber WE (2008) Diagnostic value of 123I-ioflupane and 123I-iodobenzamide SPECT scans in 248 patients with parkinsonian syndromes. Eur Neurol 59:258–266PubMedCrossRefGoogle Scholar
  90. Walter U, Niehaus L, Probst T, Benecke R, Meyer BU, Dressler D (2003) Brain parenchyma sonography discriminates Parkinson’s disease and atypical parkinsonian syndromes. Neurology 60:74–77PubMedCrossRefGoogle Scholar
  91. Walter U, Dressler D, Wolters A, Probst T, Grossmann A, Benecke R (2004) Sonographic discrimination of corticobasal degeneration vs progressive supranuclear palsy. Neurology 63:504–509PubMedCrossRefGoogle Scholar
  92. Watanabe H, Saito Y, Terao S, Ando T, Kachi T, Mukai E, Aiba I, Abe Y, Tamakoshi A, Doyu M, Hirayama M, Sobue G (2002) Progression and prognosis in multiple system atrophy: an analysis of 230 Japanese patients. Brain 125:1070–1083PubMedCrossRefGoogle Scholar
  93. Wenning G, Stefanova N (2009) Recent developments in multiple system atrophy. J Neurol 256:1791–1808PubMedCrossRefGoogle Scholar
  94. Wenning GK, Donnemiller E, Granata R, Riccabona G, Poewe W (1998) 123I-beta-CIT and 123I-IBZM-SPECT scanning in levodopa-naive Parkinson’s disease. Mov Disord 13:438–445PubMedCrossRefGoogle Scholar
  95. Williams D, Lees A (2009) Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol 8:270–279PubMedCrossRefGoogle Scholar
  96. Williams D, de Silva R, Paviour D, Pittman A, Watt H, Kilford L, Holton J, Revesz T, Lees A (2005) Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson’s syndrome and PSP-parkinsonism. Brain 128:1247–1258PubMedCrossRefGoogle Scholar
  97. Williams D, Holton J, Strand K, Revesz T, Lees A (2007) Pure akinesia with gait freezing: a third clinical phenotype of progressive supranuclear palsy. Mov Disord 22:2235–2241PubMedCrossRefGoogle Scholar
  98. Winikates J, Jankovic J (1999) Clinical correlates of vascular parkinsonism. Arch Neurol 56:98–102PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Chris C. Tang
    • 1
  • Martin Niethammer
    • 1
    • 2
  • Patricia J. Allen
    • 1
  • Klaus (Nico) L. Leenders
    • 3
  • David Eidelberg
    • 1
    • 2
  1. 1.Center for NeurosciencesThe Feinstein Institute for Medical ResearchManhassetUSA
  2. 2.Departments of Neurology and MedicineNorth Shore University HospitalManhassetUSA
  3. 3.Department of NeurologyUniversity Medical Center Groningen, University of GroningenGroningenThe Netherlands

Personalised recommendations