Skip to main content
Top
Published in: European Journal of Nuclear Medicine and Molecular Imaging 6/2012

01-06-2012 | Original Article

Progression of dopamine transporter decline in patients with the Parkinson variant of multiple system atrophy: a voxel-based analysis of [123I]β-CIT SPECT

Authors: Michael Nocker, Klaus Seppi, Eveline Donnemiller, Irene Virgolini, Gregor K. Wenning, Werner Poewe, Christoph Scherfler

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 6/2012

Login to get access

Abstract

Purpose

We characterized the progression of dopamine transporter (DAT) decline in the striatum and extrastriatal regions including the midbrain and pons of patients with the Parkinson variant of multiple system atrophy (MSA-P) and compared longitudinally collected SPECT results with those in a cohort of patients with Parkinson's disease (PD).

Methods

Eight patients with MSA-P (age 60.4 ± 7.7 years, disease duration 2.4 ± 1 years, UPDRS-III motor score 39.7 ± 4.7), and 11 patients with PD (age 61.2 ± 6.4 years, disease duration 2.4 ± 1.1 years, UPDRS-III motor score 18.9 ± 7.6) underwent a baseline and follow-up [123I]β-CIT SPECT investigation within a time period of 1.3 years. Statistical parametric mapping (SPM) and a repetitive ANOVA design were used to objectively localize the decline in DAT availability without having to make an a priori hypothesis as to its location.

Results

SPM localized significant reductions in [123I]β-CIT uptake in the dorsal brainstem of MSA-P patients compared to PD patients (p < 0.001) at baseline. Additional reductions in the DAT signal were localized in the caudate and anterior putamen of patients with MSA-P patients compared to PD patients at the follow-up examination (p < 0.001). Relative decline in tracer binding was evident in the caudate and anterior putamen of MSA-P patients compared to PD patients in the longitudinal analysis (p < 0.05), whereas no significant relative signal alteration was observed in the brainstem.

Conclusion

In contrast to PD, the relatively higher rate of signal reduction in the caudate and anterior putamen is consistent with the faster disease progression reported in MSA-P. At baseline, the tracer uptake in the brainstem was already at very low levels in the MSA-P patients compared to that in healthy control subjects and did not progress any further, suggesting that the degeneration of monoaminergic neurons is almost complete early in the disease course.
Literature
1.
go back to reference Lantos PL. The definition of multiple system atrophy: a review of recent developments. J Neuropathol Exp Neurol. 1998;57:1099–111.PubMedCrossRef Lantos PL. The definition of multiple system atrophy: a review of recent developments. J Neuropathol Exp Neurol. 1998;57:1099–111.PubMedCrossRef
2.
go back to reference Wenning GK, Tison F, Ben Shlomo Y, Daniel SE, Quinn NP. Multiple system atrophy: a review of 203 pathologically proven cases. Mov Disord. 1997;12:133–47.PubMedCrossRef Wenning GK, Tison F, Ben Shlomo Y, Daniel SE, Quinn NP. Multiple system atrophy: a review of 203 pathologically proven cases. Mov Disord. 1997;12:133–47.PubMedCrossRef
3.
go back to reference Wenning GK, Ben Shlomo Y, Magalhães M, Daniel SE, Quinn NP. Clinical features and natural history of multiple system atrophy. An analysis of 100 cases. Brain 1994;117(Pt 4):835–45.PubMedCrossRef Wenning GK, Ben Shlomo Y, Magalhães M, Daniel SE, Quinn NP. Clinical features and natural history of multiple system atrophy. An analysis of 100 cases. Brain 1994;117(Pt 4):835–45.PubMedCrossRef
4.
go back to reference Watanabe H, Saito Y, Terao S, Ando T, Kachi T, Mukai E, et al. Progression and prognosis in multiple system atrophy: an analysis of 230 Japanese patients. Brain. 2002;125:1070–83.PubMedCrossRef Watanabe H, Saito Y, Terao S, Ando T, Kachi T, Mukai E, et al. Progression and prognosis in multiple system atrophy: an analysis of 230 Japanese patients. Brain. 2002;125:1070–83.PubMedCrossRef
5.
go back to reference Ben-Shlomo Y, Wenning GK, Tison F, Quinn NP. Survival of patients with pathologically proven multiple system atrophy: a meta-analysis. Neurology. 1997;48:384–93.PubMed Ben-Shlomo Y, Wenning GK, Tison F, Quinn NP. Survival of patients with pathologically proven multiple system atrophy: a meta-analysis. Neurology. 1997;48:384–93.PubMed
6.
go back to reference Seibyl JP, Marek KL, Quinlan D, Sheff K, Zoghbi S, Zea-Ponce Y, et al. Decreased single-photon emission computed tomographic [123I]beta-CIT striatal uptake correlates with symptom severity in Parkinson's disease. Ann Neurol. 1995;38:589–98.PubMedCrossRef Seibyl JP, Marek KL, Quinlan D, Sheff K, Zoghbi S, Zea-Ponce Y, et al. Decreased single-photon emission computed tomographic [123I]beta-CIT striatal uptake correlates with symptom severity in Parkinson's disease. Ann Neurol. 1995;38:589–98.PubMedCrossRef
7.
go back to reference Brucke T, Asenbaum S, Pirker W, Djamshidian S, Wenger S, Wober C, et al. Measurement of the dopaminergic degeneration in Parkinson's disease with [123I]beta-CIT and SPECT. Correlation with clinical findings and comparison with multiple system atrophy and progressive supranuclear palsy. J Neural Transm Suppl. 1997;50:9–24.PubMed Brucke T, Asenbaum S, Pirker W, Djamshidian S, Wenger S, Wober C, et al. Measurement of the dopaminergic degeneration in Parkinson's disease with [123I]beta-CIT and SPECT. Correlation with clinical findings and comparison with multiple system atrophy and progressive supranuclear palsy. J Neural Transm Suppl. 1997;50:9–24.PubMed
8.
go back to reference Marek K, Innis R, van Dyck C, Fussell B, Early M, Eberly S, et al. [123I]beta-CIT SPECT imaging assessment of the rate of Parkinson's disease progression. Neurology. 2001;57:2089–94.PubMed Marek K, Innis R, van Dyck C, Fussell B, Early M, Eberly S, et al. [123I]beta-CIT SPECT imaging assessment of the rate of Parkinson's disease progression. Neurology. 2001;57:2089–94.PubMed
9.
go back to reference Varrone A, Marek KL, Jennings D, Innis RB, Seibyl JP. [(123)I]beta-CIT SPECT imaging demonstrates reduced density of striatal dopamine transporters in Parkinson's disease and multiple system atrophy. Mov Disord. 2001;16:1023–32.PubMedCrossRef Varrone A, Marek KL, Jennings D, Innis RB, Seibyl JP. [(123)I]beta-CIT SPECT imaging demonstrates reduced density of striatal dopamine transporters in Parkinson's disease and multiple system atrophy. Mov Disord. 2001;16:1023–32.PubMedCrossRef
10.
go back to reference Knudsen GM, Karlsborg M, Thomsen G, Krabbe K, Regeur L, Nygaard T, et al. Imaging of dopamine transporters and D2 receptors in patients with Parkinson's disease and multiple system atrophy. Eur J Nucl Med Mol Imaging. 2004;31:1631–8.PubMedCrossRef Knudsen GM, Karlsborg M, Thomsen G, Krabbe K, Regeur L, Nygaard T, et al. Imaging of dopamine transporters and D2 receptors in patients with Parkinson's disease and multiple system atrophy. Eur J Nucl Med Mol Imaging. 2004;31:1631–8.PubMedCrossRef
11.
go back to reference Scherfler C, Seppi K, Donnemiller E, Goebel G, Brenneis C, Virgolini I, et al. Voxel-wise analysis of [123I]beta-CIT SPECT differentiates the Parkinson variant of multiple system atrophy from idiopathic Parkinson's disease. Brain. 2005;128:1605–12.PubMedCrossRef Scherfler C, Seppi K, Donnemiller E, Goebel G, Brenneis C, Virgolini I, et al. Voxel-wise analysis of [123I]beta-CIT SPECT differentiates the Parkinson variant of multiple system atrophy from idiopathic Parkinson's disease. Brain. 2005;128:1605–12.PubMedCrossRef
12.
go back to reference Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology. 1967;17:427–42.PubMed Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology. 1967;17:427–42.PubMed
13.
go back to reference Fahn S, Elton R. Unified Parkinson's disease rating scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M, editors. Recent developments in Parkinson's disease. Vol. 2. Florham Park (NJ): Macmillan Health Care Information; 1987. p. 153–164. Fahn S, Elton R. Unified Parkinson's disease rating scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M, editors. Recent developments in Parkinson's disease. Vol. 2. Florham Park (NJ): Macmillan Health Care Information; 1987. p. 153–164.
14.
go back to reference Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry. 1992;55:181–4.PubMedCrossRef Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry. 1992;55:181–4.PubMedCrossRef
15.
go back to reference Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, et al. Second consensus statement on the diagnosis of multiple system atrophy. Neurology. 2008;71(9):670–6.PubMedCrossRef Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, et al. Second consensus statement on the diagnosis of multiple system atrophy. Neurology. 2008;71(9):670–6.PubMedCrossRef
16.
go back to reference Kuikka JT, Bergstrom KA, Ahonen A, Lansimies E. The dosimetry of iodine-123 labelled 2 beta-carbomethoxy-3 beta-(4-iodophenyl)tropane. Eur J Nucl Med. 1994;21:53–6.PubMed Kuikka JT, Bergstrom KA, Ahonen A, Lansimies E. The dosimetry of iodine-123 labelled 2 beta-carbomethoxy-3 beta-(4-iodophenyl)tropane. Eur J Nucl Med. 1994;21:53–6.PubMed
17.
go back to reference Laruelle M, Wallace E, Seibyl JP, Baldwin RM, Zea-Ponce Y, Zoghbi SS, et al. Graphical, kinetic, and equilibrium analyses of in vivo [123I]beta-CIT binding to dopamine transporters in healthy human subjects. J Cereb Blood Flow Metab. 1994;14:982–94.PubMedCrossRef Laruelle M, Wallace E, Seibyl JP, Baldwin RM, Zea-Ponce Y, Zoghbi SS, et al. Graphical, kinetic, and equilibrium analyses of in vivo [123I]beta-CIT binding to dopamine transporters in healthy human subjects. J Cereb Blood Flow Metab. 1994;14:982–94.PubMedCrossRef
18.
go back to reference Innis RB, Cunningham VJ, Delforge J, Fujita M, Gjedde A, Gunn RN, et al. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab. 2007;27:1533–9.PubMedCrossRef Innis RB, Cunningham VJ, Delforge J, Fujita M, Gjedde A, Gunn RN, et al. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab. 2007;27:1533–9.PubMedCrossRef
19.
go back to reference De Keyser J, De Backer JP, Ebinger G, Vauquelin G. [3H]GBR 12935 binding to dopamine uptake sites in the human brain. J Neurochem. 1989;53:1400–4.PubMedCrossRef De Keyser J, De Backer JP, Ebinger G, Vauquelin G. [3H]GBR 12935 binding to dopamine uptake sites in the human brain. J Neurochem. 1989;53:1400–4.PubMedCrossRef
20.
go back to reference Rorden C, Brett M. Stereotaxic display of brain lesions. Behav Neurol. 2000;12:191–200.PubMed Rorden C, Brett M. Stereotaxic display of brain lesions. Behav Neurol. 2000;12:191–200.PubMed
21.
go back to reference Friston KJ, Ashburner J, Frith CD, Poline JB, Heather JD, Frackowiak RS. Spatial registration and normalization of images. Hum Brain Mapp. 1995;2:165–189.CrossRef Friston KJ, Ashburner J, Frith CD, Poline JB, Heather JD, Frackowiak RS. Spatial registration and normalization of images. Hum Brain Mapp. 1995;2:165–189.CrossRef
22.
go back to reference Rakshi JS, Uema T, Ito K, Bailey DL, Morrish PK, Ashburner J, et al. Frontal, midbrain and striatal dopaminergic function in early and advanced Parkinson's disease. A 3D [(18)F]dopa-PET study. Brain. 1999;122(Pt 9):1637–50.PubMedCrossRef Rakshi JS, Uema T, Ito K, Bailey DL, Morrish PK, Ashburner J, et al. Frontal, midbrain and striatal dopaminergic function in early and advanced Parkinson's disease. A 3D [(18)F]dopa-PET study. Brain. 1999;122(Pt 9):1637–50.PubMedCrossRef
23.
go back to reference Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC. A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp. 1996;4:58–73.PubMedCrossRef Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC. A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp. 1996;4:58–73.PubMedCrossRef
24.
go back to reference Antonini A, Benti R, De Notaris R, Tesei S, Zecchinelli A, Sacilotto G, et al. 123I-Ioflupane/SPECT binding to striatal dopamine transporter (DAT) uptake in patients with Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy. Neurol Sci. 2003;24:149–50.PubMedCrossRef Antonini A, Benti R, De Notaris R, Tesei S, Zecchinelli A, Sacilotto G, et al. 123I-Ioflupane/SPECT binding to striatal dopamine transporter (DAT) uptake in patients with Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy. Neurol Sci. 2003;24:149–50.PubMedCrossRef
25.
go back to reference Pirker W, Djamshidian S, Asenbaum S, Gerschlager W, Tribl G, Hoffmann M, et al. Progression of dopaminergic degeneration in Parkinson's disease and atypical parkinsonism: a longitudinal beta-CIT SPECT study. Mov Disord. 2002;17:45–53.PubMedCrossRef Pirker W, Djamshidian S, Asenbaum S, Gerschlager W, Tribl G, Hoffmann M, et al. Progression of dopaminergic degeneration in Parkinson's disease and atypical parkinsonism: a longitudinal beta-CIT SPECT study. Mov Disord. 2002;17:45–53.PubMedCrossRef
26.
go back to reference Scherfler C, Nocker M. Dopamine transporter SPECT: how to remove subjectivity? Mov Disord. 2009;24 Suppl 2:S721–4.PubMedCrossRef Scherfler C, Nocker M. Dopamine transporter SPECT: how to remove subjectivity? Mov Disord. 2009;24 Suppl 2:S721–4.PubMedCrossRef
27.
go back to reference Kim YJ, Ichise M, Ballinger JR, Vines D, Erami SS, Tatschida T, et al. Combination of dopamine transporter and D2 receptor SPECT in the diagnostic evaluation of PD, MSA, and PSP. Mov Disord. 2002;17:303–12.PubMedCrossRef Kim YJ, Ichise M, Ballinger JR, Vines D, Erami SS, Tatschida T, et al. Combination of dopamine transporter and D2 receptor SPECT in the diagnostic evaluation of PD, MSA, and PSP. Mov Disord. 2002;17:303–12.PubMedCrossRef
28.
go back to reference Brooks DJ, Salmon EP, Mathias CJ, Quinn N, Leenders KL, Bannister R, et al. The relationship between locomotor disability, autonomic dysfunction, and the integrity of the striatal dopaminergic system in patients with multiple system atrophy, pure autonomic failure, and Parkinson's disease, studied with PET. Brain. 1990;1990:1539–52.CrossRef Brooks DJ, Salmon EP, Mathias CJ, Quinn N, Leenders KL, Bannister R, et al. The relationship between locomotor disability, autonomic dysfunction, and the integrity of the striatal dopaminergic system in patients with multiple system atrophy, pure autonomic failure, and Parkinson's disease, studied with PET. Brain. 1990;1990:1539–52.CrossRef
29.
go back to reference Kume A, Takahashi A, Hashizume Y. Neuronal cell loss of the striatonigral system in multiple system atrophy. J Neurol Sci. 1993;117:33–40.PubMedCrossRef Kume A, Takahashi A, Hashizume Y. Neuronal cell loss of the striatonigral system in multiple system atrophy. J Neurol Sci. 1993;117:33–40.PubMedCrossRef
30.
go back to reference Morrish PK, Sawle GV, Brooks DJ. The rate of progression of Parkinson's disease. A longitudinal [18F]DOPA PET study. Adv Neurol. 1996;69:427–31.PubMed Morrish PK, Sawle GV, Brooks DJ. The rate of progression of Parkinson's disease. A longitudinal [18F]DOPA PET study. Adv Neurol. 1996;69:427–31.PubMed
31.
go back to reference Parkinson Study Group. Dopamine transporter brain imaging to assess the effects of pramipexole vs levodopa on Parkinson disease progression. JAMA. 2002;287(13):1653–61.CrossRef Parkinson Study Group. Dopamine transporter brain imaging to assess the effects of pramipexole vs levodopa on Parkinson disease progression. JAMA. 2002;287(13):1653–61.CrossRef
32.
go back to reference Seibyl JP, Marek K, Sheff K, Baldwin RM, Zoghbi S, Zea-Ponce Y, et al. Test/retest reproducibility of iodine-123-betaCIT SPECT brain measurement of dopamine transporters in Parkinson's patients. J Nucl Med. 1997;38:1453–9.PubMed Seibyl JP, Marek K, Sheff K, Baldwin RM, Zoghbi S, Zea-Ponce Y, et al. Test/retest reproducibility of iodine-123-betaCIT SPECT brain measurement of dopamine transporters in Parkinson's patients. J Nucl Med. 1997;38:1453–9.PubMed
33.
go back to reference Booij J, Habraken JB, Bergmans P, Tissingh G, Winogrodzka A, Wolters EC, et al. Imaging of dopamine transporters with iodine-123-FP-CIT SPECT in healthy controls and patients with Parkinson's disease. J Nucl Med. 1998;39:1879–84.PubMed Booij J, Habraken JB, Bergmans P, Tissingh G, Winogrodzka A, Wolters EC, et al. Imaging of dopamine transporters with iodine-123-FP-CIT SPECT in healthy controls and patients with Parkinson's disease. J Nucl Med. 1998;39:1879–84.PubMed
34.
go back to reference Morrish PK. How valid is dopamine transporter imaging as a surrogate marker in research trials in Parkinson’s disease. Mov Disord. 2003;18: Suppl 7:S63–70.PubMedCrossRef Morrish PK. How valid is dopamine transporter imaging as a surrogate marker in research trials in Parkinson’s disease. Mov Disord. 2003;18: Suppl 7:S63–70.PubMedCrossRef
35.
go back to reference Seppi K, Scherfler C, Donnemiller E, Virgolini I, Schocke MF, Goebel G, et al. Topography of dopamine transporter availability in progressive supranuclear palsy: a voxelwise [123I]beta-CIT SPECT analysis. Arch Neurol. 2006;63:1154–60.PubMedCrossRef Seppi K, Scherfler C, Donnemiller E, Virgolini I, Schocke MF, Goebel G, et al. Topography of dopamine transporter availability in progressive supranuclear palsy: a voxelwise [123I]beta-CIT SPECT analysis. Arch Neurol. 2006;63:1154–60.PubMedCrossRef
36.
go back to reference Innis R, Baldwin R, Sybirska E, Zea Y, Laruelle M, al-Tikriti M, et al. Single photon emission computed tomography imaging of monoamine reuptake sites in primate brain with [123I]CIT. Eur J Pharmacol. 1991;200:369–70.PubMedCrossRef Innis R, Baldwin R, Sybirska E, Zea Y, Laruelle M, al-Tikriti M, et al. Single photon emission computed tomography imaging of monoamine reuptake sites in primate brain with [123I]CIT. Eur J Pharmacol. 1991;200:369–70.PubMedCrossRef
37.
go back to reference Staley JK, Basile M, Flynn DD, Mash DC. Visualizing dopamine and serotonin transporters in the human brain with the potent cocaine analogue [125I]RTI-55: in vitro binding and autoradiographic characterization. J Neurochem. 1994;62:549–56.PubMedCrossRef Staley JK, Basile M, Flynn DD, Mash DC. Visualizing dopamine and serotonin transporters in the human brain with the potent cocaine analogue [125I]RTI-55: in vitro binding and autoradiographic characterization. J Neurochem. 1994;62:549–56.PubMedCrossRef
38.
go back to reference Pirker W, Asenbaum S, Kasper S, Walter H, Angelberger P, Koch G, et al. beta-CIT SPECT demonstrates blockade of 5HT-uptake sites by citalopram in the human brain in vivo. J Neural Transm Gen Sect. 1995;100:247–56.PubMedCrossRef Pirker W, Asenbaum S, Kasper S, Walter H, Angelberger P, Koch G, et al. beta-CIT SPECT demonstrates blockade of 5HT-uptake sites by citalopram in the human brain in vivo. J Neural Transm Gen Sect. 1995;100:247–56.PubMedCrossRef
39.
go back to reference Uhl GR. Neurotransmitter transporters (plus): a promising new gene family. Trends Neurosci. 1992;15:265–8.PubMedCrossRef Uhl GR. Neurotransmitter transporters (plus): a promising new gene family. Trends Neurosci. 1992;15:265–8.PubMedCrossRef
40.
41.
go back to reference Papp MI, Lantos PL. The distribution of oligodendroglial inclusions in multiple system atrophy and its relevance to clinical symptomatology. Brain. 1994;117(Pt 2):235–43.PubMedCrossRef Papp MI, Lantos PL. The distribution of oligodendroglial inclusions in multiple system atrophy and its relevance to clinical symptomatology. Brain. 1994;117(Pt 2):235–43.PubMedCrossRef
42.
go back to reference Benarroch EE, Schmeichel AM, Low PA, Parisi JE. Involvement of medullary serotonergic groups in multiple system atrophy. Ann Neurol. 2004;55:418–22.PubMedCrossRef Benarroch EE, Schmeichel AM, Low PA, Parisi JE. Involvement of medullary serotonergic groups in multiple system atrophy. Ann Neurol. 2004;55:418–22.PubMedCrossRef
43.
go back to reference Glover G, Pelc N. The nonlinear partial volume artefact. J Comput Assist Tomogr. 1979;25:79–86. Glover G, Pelc N. The nonlinear partial volume artefact. J Comput Assist Tomogr. 1979;25:79–86.
44.
go back to reference Hoffman EJ, Huang SC, Phelps ME. Quantification in positron emission tomography. 1. Effect of object size. J Comput Assist Tomogr. 1979;22:324–33. Hoffman EJ, Huang SC, Phelps ME. Quantification in positron emission tomography. 1. Effect of object size. J Comput Assist Tomogr. 1979;22:324–33.
45.
go back to reference Kojima A, Matsumoto M, Takahashi M, Hirota Y, Yoshida H. Effect of spatial resolution on SPECT quantification values. J Nucl Med. 1989;30:508–14.PubMed Kojima A, Matsumoto M, Takahashi M, Hirota Y, Yoshida H. Effect of spatial resolution on SPECT quantification values. J Nucl Med. 1989;30:508–14.PubMed
46.
go back to reference Pirker W, Holler I, Gerschlager W, Asenbaum S, Zettinig G, Brucke T. Measuring the rate of progression of Parkinson's disease over a 5-year period with beta-CIT SPECT. Mov Disord. 2003;18:1266–72.PubMedCrossRef Pirker W, Holler I, Gerschlager W, Asenbaum S, Zettinig G, Brucke T. Measuring the rate of progression of Parkinson's disease over a 5-year period with beta-CIT SPECT. Mov Disord. 2003;18:1266–72.PubMedCrossRef
47.
go back to reference Muller J, Wenning GK, Jellinger K, McKee A, Poewe W, Litvan I. Progression of Hoehn and Yahr stages in Parkinsonian disorders: a clinicopathologic study. Neurology. 2000;55:888–91.PubMed Muller J, Wenning GK, Jellinger K, McKee A, Poewe W, Litvan I. Progression of Hoehn and Yahr stages in Parkinsonian disorders: a clinicopathologic study. Neurology. 2000;55:888–91.PubMed
48.
go back to reference Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, et al. Variable expression of Parkinson's disease: a base-line analysis of the DATATOP cohort. The Parkinson Study Group Neurology. 1990;40:1529–34.PubMed Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, et al. Variable expression of Parkinson's disease: a base-line analysis of the DATATOP cohort. The Parkinson Study Group Neurology. 1990;40:1529–34.PubMed
Metadata
Title
Progression of dopamine transporter decline in patients with the Parkinson variant of multiple system atrophy: a voxel-based analysis of [123I]β-CIT SPECT
Authors
Michael Nocker
Klaus Seppi
Eveline Donnemiller
Irene Virgolini
Gregor K. Wenning
Werner Poewe
Christoph Scherfler
Publication date
01-06-2012
Publisher
Springer-Verlag
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 6/2012
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-012-2100-5

Other articles of this Issue 6/2012

European Journal of Nuclear Medicine and Molecular Imaging 6/2012 Go to the issue