Skip to main content
Top
Published in: European Journal of Nuclear Medicine and Molecular Imaging 7/2007

01-07-2007 | Original article

Identification by [99mTc]ECD SPECT of anterior cingulate hypoperfusion in progressive supranuclear palsy, in comparison with Parkinson’s disease

Authors: Andrea Varrone, Marco Pagani, Elena Salvatore, Dario Salmaso, Valeria Sansone, Marianna Amboni, Flavio Nobili, Giuseppe De Michele, Alessandro Filla, Paolo Barone, Sabina Pappatà, Marco Salvatore

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 7/2007

Login to get access

Abstract

Purpose

Progressive supranuclear palsy (PSP) is an akinetic-rigid syndrome that can be difficult to differentiate from Parkinson’s disease (PD), particularly at an early stage. [99mTc]ethyl cysteinate dimer (ECD) SPECT could represent a widely available tool to assist in the differential diagnosis. In this study we used voxel-based analysis and Computerised Brain Atlas (CBA)-based principal component analysis (PCA) of [99mTc]ECD SPECT data to test whether: (1) specific patterns of rCBF abnormalities can differentiate PSP from controls and PD; (2) networks of dysfunctional brain regions can be found in PSP vs controls and PD.

Methods

Nine PD patients, 16 PSP patients and ten controls were studied with [99mTc]ECD SPECT using a brain-dedicated device (Ceraspect). Voxel-based analysis was performed with statistical parametric mapping. PCA was applied to volume of interest data after spatial normalisation to CBA.

Results

The voxel-based analysis showed hypoperfusion of the anterior cingulate and medial frontal cortex in PSP compared with controls and PD. In PSP patients the rCBF impairment extended to the pre-supplementary motor area and prefrontal cortex, areas involved in executive function and motor networks. Compared with PSP patients, PD patients showed a mild rCBF decrease in associative visual areas which could be related to the known impairment of visuospatial function. The PCA identified three principal components differentiating PSP patients from controls and/or PD patients that included groups of cortical and subcortical brain regions with relatively decreased (cingulate cortex, prefrontal cortex and caudate) or increased (parietal cortex) rCBF, representing distinct functional networks in PSP.

Conclusion

Anterior cingulate hypoperfusion seems to be an early, distinct brain abnormality in PSP as compared with PD.
Literature
1.
go back to reference Litvan I, Campbell G, Mangone CA, Verny M, McKee A, Chaudhuri KR, et al. Which clinical features differentiate progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) from related disorders? A clinicopathological study. Brain 1997;120 Pt 1:65–74.PubMedCrossRef Litvan I, Campbell G, Mangone CA, Verny M, McKee A, Chaudhuri KR, et al. Which clinical features differentiate progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) from related disorders? A clinicopathological study. Brain 1997;120 Pt 1:65–74.PubMedCrossRef
2.
go back to reference Litvan I, Agid Y, Jankovic J, Goetz C, Brandel JP, Lai EC, et al. Accuracy of clinical criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). Neurology 1996;46:922–30.PubMed Litvan I, Agid Y, Jankovic J, Goetz C, Brandel JP, Lai EC, et al. Accuracy of clinical criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). Neurology 1996;46:922–30.PubMed
3.
go back to reference Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 1996;47:1–9.PubMed Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 1996;47:1–9.PubMed
4.
go back to reference Williams DR, de Silva R, Paviour DC, Pittman A, Watt HC, Kilford L, et al. Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson’s syndrome and PSP-parkinsonism. Brain 2005;128:1247–58.PubMedCrossRef Williams DR, de Silva R, Paviour DC, Pittman A, Watt HC, Kilford L, et al. Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson’s syndrome and PSP-parkinsonism. Brain 2005;128:1247–58.PubMedCrossRef
5.
go back to reference D’Antona R, Baron JC, Samson Y, Serdaru M, Viader F, Agid Y, et al. Subcortical dementia. Frontal cortex hypometabolism detected by positron tomography in patients with progressive supranuclear palsy. Brain 1985;108 Pt 3:785–99.PubMedCrossRef D’Antona R, Baron JC, Samson Y, Serdaru M, Viader F, Agid Y, et al. Subcortical dementia. Frontal cortex hypometabolism detected by positron tomography in patients with progressive supranuclear palsy. Brain 1985;108 Pt 3:785–99.PubMedCrossRef
6.
go back to reference Foster NL, Gilman S, Berent S, Morin EM, Brown MB, Koeppe RA. Cerebral hypometabolism in progressive supranuclear palsy studied with positron emission tomography. Ann Neurol 1988;24:399–406.PubMedCrossRef Foster NL, Gilman S, Berent S, Morin EM, Brown MB, Koeppe RA. Cerebral hypometabolism in progressive supranuclear palsy studied with positron emission tomography. Ann Neurol 1988;24:399–406.PubMedCrossRef
7.
go back to reference Brooks DJ, Ibanez V, Sawle GV, Playford ED, Quinn N, Mathias CJ, et al. Striatal D2 receptor status in patients with Parkinson’s disease, striatonigral degeneration, and progressive supranuclear palsy, measured with 11C-raclopride and positron emission tomography. Ann Neurol 1992;31:184–92.PubMedCrossRef Brooks DJ, Ibanez V, Sawle GV, Playford ED, Quinn N, Mathias CJ, et al. Striatal D2 receptor status in patients with Parkinson’s disease, striatonigral degeneration, and progressive supranuclear palsy, measured with 11C-raclopride and positron emission tomography. Ann Neurol 1992;31:184–92.PubMedCrossRef
8.
go back to reference Blin J, Baron JC, Dubois B, Pillon B, Cambon H, Cambier J, et al. Positron emission tomography study in progressive supranuclear palsy. Brain hypometabolic pattern and clinicometabolic correlations. Arch Neurol 1990;47:747–52.PubMed Blin J, Baron JC, Dubois B, Pillon B, Cambon H, Cambier J, et al. Positron emission tomography study in progressive supranuclear palsy. Brain hypometabolic pattern and clinicometabolic correlations. Arch Neurol 1990;47:747–52.PubMed
9.
go back to reference Garraux G, Salmon E, Degueldre C, Lemaire C, Laureys S, Franck G. Comparison of impaired subcortico-frontal metabolic networks in normal aging, subcortico-frontal dementia, and cortical frontal dementia. Neuroimage 1999;10:149–62.PubMedCrossRef Garraux G, Salmon E, Degueldre C, Lemaire C, Laureys S, Franck G. Comparison of impaired subcortico-frontal metabolic networks in normal aging, subcortico-frontal dementia, and cortical frontal dementia. Neuroimage 1999;10:149–62.PubMedCrossRef
10.
go back to reference Salmon E, Van der Linden MV, Franck G. Anterior cingulate and motor network metabolic impairment in progressive supranuclear palsy. Neuroimage 1997;5:173–8.PubMedCrossRef Salmon E, Van der Linden MV, Franck G. Anterior cingulate and motor network metabolic impairment in progressive supranuclear palsy. Neuroimage 1997;5:173–8.PubMedCrossRef
11.
go back to reference Eckert T, Barnes A, Dhawan V, Frucht S, Gordon MF, Feigin AS, et al. FDG PET in the differential diagnosis of parkinsonian disorders. Neuroimage 2005;26:912–21.PubMedCrossRef Eckert T, Barnes A, Dhawan V, Frucht S, Gordon MF, Feigin AS, et al. FDG PET in the differential diagnosis of parkinsonian disorders. Neuroimage 2005;26:912–21.PubMedCrossRef
12.
go back to reference Klein RC, de Jong BM, de Vries JJ, Leenders KL. Direct comparison between regional cerebral metabolism in progressive supranuclear palsy and Parkinson’s disease. Mov Disord 2005;20:1021–30.PubMedCrossRef Klein RC, de Jong BM, de Vries JJ, Leenders KL. Direct comparison between regional cerebral metabolism in progressive supranuclear palsy and Parkinson’s disease. Mov Disord 2005;20:1021–30.PubMedCrossRef
13.
go back to reference Burn DJ, Rinne JO, Quinn NP, Lees AJ, Marsden CD, Brooks DJ. Striatal opioid receptor binding in Parkinson’s disease, striatonigral degeneration and Steele-Richardson-Olszewski syndrome: a [11C]diprenorphine PET study. Brain 1995;118 Pt 4:951–8.PubMedCrossRef Burn DJ, Rinne JO, Quinn NP, Lees AJ, Marsden CD, Brooks DJ. Striatal opioid receptor binding in Parkinson’s disease, striatonigral degeneration and Steele-Richardson-Olszewski syndrome: a [11C]diprenorphine PET study. Brain 1995;118 Pt 4:951–8.PubMedCrossRef
14.
go back to reference Shinotoh H, Namba H, Yamaguchi M, Fukushi K, Nagatsuka S, Iyo M, et al. Positron emission tomographic measurement of acetylcholinesterase activity reveals differential loss of ascending cholinergic systems in Parkinson’s disease and progressive supranuclear palsy. Ann Neurol 1999;46:62–9.PubMedCrossRef Shinotoh H, Namba H, Yamaguchi M, Fukushi K, Nagatsuka S, Iyo M, et al. Positron emission tomographic measurement of acetylcholinesterase activity reveals differential loss of ascending cholinergic systems in Parkinson’s disease and progressive supranuclear palsy. Ann Neurol 1999;46:62–9.PubMedCrossRef
15.
go back to reference Messa C, Volonte MA, Fazio F, Zito F, Carpinelli A, d’Amico A, et al. Differential distribution of striatal [123I]beta-CIT in Parkinson’s disease and progressive supranuclear palsy, evaluated with single-photon emission tomography. Eur J Nucl Med 1998;25:1270–6.PubMedCrossRef Messa C, Volonte MA, Fazio F, Zito F, Carpinelli A, d’Amico A, et al. Differential distribution of striatal [123I]beta-CIT in Parkinson’s disease and progressive supranuclear palsy, evaluated with single-photon emission tomography. Eur J Nucl Med 1998;25:1270–6.PubMedCrossRef
16.
go back to reference Ilgin N, Zubieta J, Reich SG, Dannals RF, Ravert HT, Frost JJ. PET imaging of the dopamine transporter in progressive supranuclear palsy and Parkinson’s disease. Neurology 1999;52:1221–6.PubMed Ilgin N, Zubieta J, Reich SG, Dannals RF, Ravert HT, Frost JJ. PET imaging of the dopamine transporter in progressive supranuclear palsy and Parkinson’s disease. Neurology 1999;52:1221–6.PubMed
17.
go back to reference Oyanagi C, Katsumi Y, Hanakawa T, Hayashi T, Thuy DD, Hashikawa K, et al. Comparison of striatal dopamine D2 receptors in Parkinson’s disease and progressive supranuclear palsy patients using [123I] iodobenzofuran single-photon emission computed tomography. J Neuroimaging 2002;12:316–24.PubMedCrossRef Oyanagi C, Katsumi Y, Hanakawa T, Hayashi T, Thuy DD, Hashikawa K, et al. Comparison of striatal dopamine D2 receptors in Parkinson’s disease and progressive supranuclear palsy patients using [123I] iodobenzofuran single-photon emission computed tomography. J Neuroimaging 2002;12:316–24.PubMedCrossRef
18.
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
19.
go back to reference Defebvre L, Lecouffe P, Destee A, Houdart P, Steinling M. Tomographic measurements of regional cerebral blood flow in progressive supranuclear palsy and Parkinson’s disease. Acta Neurol Scand 1995;92:235–41.PubMedCrossRef Defebvre L, Lecouffe P, Destee A, Houdart P, Steinling M. Tomographic measurements of regional cerebral blood flow in progressive supranuclear palsy and Parkinson’s disease. Acta Neurol Scand 1995;92:235–41.PubMedCrossRef
20.
go back to reference Zhang L, Murata Y, Ishida R, Saitoh Y, Mizusawa H, Shibuya H. Differentiating between progressive supranuclear palsy and corticobasal degeneration by brain perfusion SPET. Nucl Med Commun 2001;22:767–72.PubMedCrossRef Zhang L, Murata Y, Ishida R, Saitoh Y, Mizusawa H, Shibuya H. Differentiating between progressive supranuclear palsy and corticobasal degeneration by brain perfusion SPET. Nucl Med Commun 2001;22:767–72.PubMedCrossRef
21.
go back to reference Van Laere K, Casteels C, De Ceuninck L, Vanbilloen B, Maes A, Mortelmans L, et al. Dual-tracer dopamine transporter and perfusion SPECT in differential diagnosis of parkinsonism using template-based discriminant analysis. J Nucl Med 2006;47:384–92.PubMed Van Laere K, Casteels C, De Ceuninck L, Vanbilloen B, Maes A, Mortelmans L, et al. Dual-tracer dopamine transporter and perfusion SPECT in differential diagnosis of parkinsonism using template-based discriminant analysis. J Nucl Med 2006;47:384–92.PubMed
22.
go back to reference Eidelberg D, Moeller JR, Dhawan V, Sidtis JJ, Ginos JZ, Strother SC, et al. The metabolic anatomy of Parkinson’s disease: complementary [18F]fluorodeoxyglucose and [18F]fluorodopa positron emission tomographic studies. Mov Disord 1990;5:203–13.PubMedCrossRef Eidelberg D, Moeller JR, Dhawan V, Sidtis JJ, Ginos JZ, Strother SC, et al. The metabolic anatomy of Parkinson’s disease: complementary [18F]fluorodeoxyglucose and [18F]fluorodopa positron emission tomographic studies. Mov Disord 1990;5:203–13.PubMedCrossRef
23.
go back to reference Eidelberg D, Moeller JR, Dhawan V, Spetsieris P, Takikawa S, Ishikawa T, et al. The metabolic topography of parkinsonism. J Cereb Blood Flow Metab 1994;14:783–801.PubMed Eidelberg D, Moeller JR, Dhawan V, Spetsieris P, Takikawa S, Ishikawa T, et al. The metabolic topography of parkinsonism. J Cereb Blood Flow Metab 1994;14:783–801.PubMed
24.
go back to reference Lozza C, Baron JC, Eidelberg D, Mentis MJ, Carbon M, Marie RM. Executive processes in Parkinson’s disease: FDG-PET and network analysis. Hum Brain Mapp 2004;22:236–45.PubMedCrossRef Lozza C, Baron JC, Eidelberg D, Mentis MJ, Carbon M, Marie RM. Executive processes in Parkinson’s disease: FDG-PET and network analysis. Hum Brain Mapp 2004;22:236–45.PubMedCrossRef
25.
go back to reference Gibb WR, Lees AJ. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 1988;51:745–52.PubMedCrossRef Gibb WR, Lees AJ. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 1988;51:745–52.PubMedCrossRef
26.
go back to reference Van Laere K, Santens P, Bosman T, De Reuck J, Mortelmans L, Dierckx R. Statistical parametric mapping of 99mTc-ECD SPECT in idiopathic Parkinson’s disease and multiple system atrophy with predominant parkinsonian features: correlation with clinical parameters. J Nucl Med 2004;45:933–42.PubMed Van Laere K, Santens P, Bosman T, De Reuck J, Mortelmans L, Dierckx R. Statistical parametric mapping of 99mTc-ECD SPECT in idiopathic Parkinson’s disease and multiple system atrophy with predominant parkinsonian features: correlation with clinical parameters. J Nucl Med 2004;45:933–42.PubMed
27.
go back to reference Greitz T, Bohm C, Holte S, Eriksson L. A computerized brain atlas: construction, anatomical content, and some applications. J Comput Assist Tomogr 1991;15:26–38.PubMedCrossRef Greitz T, Bohm C, Holte S, Eriksson L. A computerized brain atlas: construction, anatomical content, and some applications. J Comput Assist Tomogr 1991;15:26–38.PubMedCrossRef
28.
go back to reference Thurfjell L, Bohm C, Bengtsson E. CBA—an atlas-based software tool used to facilitate the interpretation of neuroimaging data. Comput Methods Programs Biomed 1995;47:51–71.PubMedCrossRef Thurfjell L, Bohm C, Bengtsson E. CBA—an atlas-based software tool used to facilitate the interpretation of neuroimaging data. Comput Methods Programs Biomed 1995;47:51–71.PubMedCrossRef
29.
go back to reference Pett M, Lackey N, Sullivan J. Making sense of factor analysis: a practical guide to understanding factor analysis for instrument development in health care research. Thousand Oaks, CA: Sage Publication, Inc.; 2003. Pett M, Lackey N, Sullivan J. Making sense of factor analysis: a practical guide to understanding factor analysis for instrument development in health care research. Thousand Oaks, CA: Sage Publication, Inc.; 2003.
30.
go back to reference Hosaka K, Ishii K, Sakamoto S, Mori T, Sasaki M, Hirono N, et al. Voxel-based comparison of regional cerebral glucose metabolism between PSP and corticobasal degeneration. J Neurol Sci 2002;199:67–71.PubMedCrossRef Hosaka K, Ishii K, Sakamoto S, Mori T, Sasaki M, Hirono N, et al. Voxel-based comparison of regional cerebral glucose metabolism between PSP and corticobasal degeneration. J Neurol Sci 2002;199:67–71.PubMedCrossRef
31.
go back to reference Badgaiyan RD. Executive control, willed actions, and nonconscious processing. Hum Brain Mapp 2000;9:38–41.PubMedCrossRef Badgaiyan RD. Executive control, willed actions, and nonconscious processing. Hum Brain Mapp 2000;9:38–41.PubMedCrossRef
32.
go back to reference Pardo JV, Pardo PJ, Janer KW, Raichle ME. The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. Proc Natl Acad Sci USA 1990;87:256–59.PubMedCrossRef Pardo JV, Pardo PJ, Janer KW, Raichle ME. The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. Proc Natl Acad Sci USA 1990;87:256–59.PubMedCrossRef
33.
go back to reference Carter CS, Mintun M, Cohen JD. Interference and facilitation effects during selective attention: an H2 15O PET study of Stroop task performance. Neuroimage 1995;2:264–72.PubMedCrossRef Carter CS, Mintun M, Cohen JD. Interference and facilitation effects during selective attention: an H2 15O PET study of Stroop task performance. Neuroimage 1995;2:264–72.PubMedCrossRef
34.
go back to reference Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain 1995;118 Pt 1:279–306.PubMedCrossRef Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain 1995;118 Pt 1:279–306.PubMedCrossRef
35.
go back to reference Morris J, Dolan R. Functional Neuroanatomy of human emotion. In: Frackowiak RSJ, Friston FK, Frith CD, Dolan RJ, Zeki S, Price CJ,editors. Human brain function. 2nd ed. San Diego: Elsevier Academic Press; 2004. pp 365–96. Morris J, Dolan R. Functional Neuroanatomy of human emotion. In: Frackowiak RSJ, Friston FK, Frith CD, Dolan RJ, Zeki S, Price CJ,editors. Human brain function. 2nd ed. San Diego: Elsevier Academic Press; 2004. pp 365–96.
36.
go back to reference Frith C, Gallagher H, Maguire E. Mechanisms of control, Chapter 18. In: Frackowiak RSJ, Friston KJ, Frith CD, Dolan RJ, Zeki S, Price CJ, editors. Human brain function. 2nd ed. San Diego: Elsevier; 2004. pp 329–62. Frith C, Gallagher H, Maguire E. Mechanisms of control, Chapter 18. In: Frackowiak RSJ, Friston KJ, Frith CD, Dolan RJ, Zeki S, Price CJ, editors. Human brain function. 2nd ed. San Diego: Elsevier; 2004. pp 329–62.
37.
go back to reference Migneco O, Benoit M, Koulibaly PM, Dygai I, Bertogliati C, Desvignes P, et al. Perfusion brain SPECT and statistical parametric mapping analysis indicate that apathy is a cingulate syndrome: a study in Alzheimer’s disease and nondemented patients. Neuroimage 2001;13:896–902.PubMedCrossRef Migneco O, Benoit M, Koulibaly PM, Dygai I, Bertogliati C, Desvignes P, et al. Perfusion brain SPECT and statistical parametric mapping analysis indicate that apathy is a cingulate syndrome: a study in Alzheimer’s disease and nondemented patients. Neuroimage 2001;13:896–902.PubMedCrossRef
38.
go back to reference Foster NL, Minoshima S, Johanns J, Little R, Heumann ML, Kuhl DE, et al. PET measures of benzodiazepine receptors in progressive supranuclear palsy. Neurology 2000;54:1768–73.PubMed Foster NL, Minoshima S, Johanns J, Little R, Heumann ML, Kuhl DE, et al. PET measures of benzodiazepine receptors in progressive supranuclear palsy. Neurology 2000;54:1768–73.PubMed
39.
go back to reference Abe Y, Kachi T, Kato T, Arahata Y, Yamada T, Washimi Y, et al. Occipital hypoperfusion in Parkinson’s disease without dementia: correlation to impaired cortical visual processing. J Neurol Neurosurg Psychiatry 2003;74:419–22.PubMedCrossRef Abe Y, Kachi T, Kato T, Arahata Y, Yamada T, Washimi Y, et al. Occipital hypoperfusion in Parkinson’s disease without dementia: correlation to impaired cortical visual processing. J Neurol Neurosurg Psychiatry 2003;74:419–22.PubMedCrossRef
40.
go back to reference Juh R, Kim J, Moon D, Choe B, Suh T. Different metabolic patterns analysis of Parkinsonism on the 18F-FDG PET. Eur J Radiol 2004;51:223–33.PubMedCrossRef Juh R, Kim J, Moon D, Choe B, Suh T. Different metabolic patterns analysis of Parkinsonism on the 18F-FDG PET. Eur J Radiol 2004;51:223–33.PubMedCrossRef
41.
go back to reference Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986;9:357–81.PubMedCrossRef Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986;9:357–81.PubMedCrossRef
42.
go back to reference Middleton FA, Strick PL. Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies. Brain Cogn 2000;42:183–200.PubMedCrossRef Middleton FA, Strick PL. Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies. Brain Cogn 2000;42:183–200.PubMedCrossRef
43.
go back to reference Franceschi M, Anchisi D, Pelati O, Zuffi M, Matarrese M, Moresco RM, et al. Glucose metabolism and serotonin receptors in the frontotemporal lobe degeneration. Ann Neurol 2005;57:216–25.PubMedCrossRef Franceschi M, Anchisi D, Pelati O, Zuffi M, Matarrese M, Moresco RM, et al. Glucose metabolism and serotonin receptors in the frontotemporal lobe degeneration. Ann Neurol 2005;57:216–25.PubMedCrossRef
44.
go back to reference Minoshima S, Giordani B, Berent S, Frey KA, Foster NL, Kuhl DE. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer’s disease. Ann Neurol 1997; 42:85–94.PubMedCrossRef Minoshima S, Giordani B, Berent S, Frey KA, Foster NL, Kuhl DE. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer’s disease. Ann Neurol 1997; 42:85–94.PubMedCrossRef
45.
go back to reference Lopez OL, Litvan I, Catt KE, Stowe R, Klunk W, Kaufer DI, et al. Accuracy of four clinical diagnostic criteria for the diagnosis of neurodegenerative dementias. Neurology 1999;53:1292–9.PubMed Lopez OL, Litvan I, Catt KE, Stowe R, Klunk W, Kaufer DI, et al. Accuracy of four clinical diagnostic criteria for the diagnosis of neurodegenerative dementias. Neurology 1999;53:1292–9.PubMed
46.
go back to reference Brenneis C, Seppi K, Schocke M, Benke T, Wenning GK, Poewe W. Voxel based morphometry reveals a distinct pattern of frontal atrophy in progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 2004;75:246–9.PubMed Brenneis C, Seppi K, Schocke M, Benke T, Wenning GK, Poewe W. Voxel based morphometry reveals a distinct pattern of frontal atrophy in progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 2004;75:246–9.PubMed
47.
go back to reference Price S, Paviour D, Scahill R, Stevens J, Rossor M, Lees A, et al. Voxel-based morphometry detects patterns of atrophy that help differentiate progressive supranuclear palsy and Parkinson’s disease. Neuroimage 2004;23:663–9.PubMedCrossRef Price S, Paviour D, Scahill R, Stevens J, Rossor M, Lees A, et al. Voxel-based morphometry detects patterns of atrophy that help differentiate progressive supranuclear palsy and Parkinson’s disease. Neuroimage 2004;23:663–9.PubMedCrossRef
48.
go back to reference Cordato NJ, Duggins AJ, Halliday GM, Morris JG, Pantelis C. Clinical deficits correlate with regional cerebral atrophy in progressive supranuclear palsy. Brain 2005;128:1259–66.PubMedCrossRef Cordato NJ, Duggins AJ, Halliday GM, Morris JG, Pantelis C. Clinical deficits correlate with regional cerebral atrophy in progressive supranuclear palsy. Brain 2005;128:1259–66.PubMedCrossRef
Metadata
Title
Identification by [99mTc]ECD SPECT of anterior cingulate hypoperfusion in progressive supranuclear palsy, in comparison with Parkinson’s disease
Authors
Andrea Varrone
Marco Pagani
Elena Salvatore
Dario Salmaso
Valeria Sansone
Marianna Amboni
Flavio Nobili
Giuseppe De Michele
Alessandro Filla
Paolo Barone
Sabina Pappatà
Marco Salvatore
Publication date
01-07-2007
Publisher
Springer-Verlag
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 7/2007
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-006-0344-7

Other articles of this Issue 7/2007

European Journal of Nuclear Medicine and Molecular Imaging 7/2007 Go to the issue

Letter to the editor

Reply