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Published in: Journal of Neurology 7/2019

Open Access 01-07-2019 | Parkinson's Disease | Original Communication

Classification of degenerative parkinsonism subtypes by support-vector-machine analysis and striatal 123I-FP-CIT indices

Authors: Nicolas Nicastro, Jennifer Wegrzyk, Maria Giulia Preti, Vanessa Fleury, Dimitri Van de Ville, Valentina Garibotto, Pierre R. Burkhard

Published in: Journal of Neurology | Issue 7/2019

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Abstract

Objectives

To provide an automated classification method for degenerative parkinsonian syndromes (PS) based on semiquantitative 123I-FP-CIT SPECT striatal indices and support-vector-machine (SVM) analysis.

Methods

123I-FP-CIT SPECT was performed at a single-center level on 370 individuals with PS, including 280 patients with Parkinson’s disease (PD), 21 with multiple system atrophy-parkinsonian type (MSA-P), 41 with progressive supranuclear palsy (PSP) and 28 with corticobasal syndrome (CBS) (mean age 70.3 years, 47% female, mean disease duration at scan 1.4 year), as well as 208 age- and gender-matched control subjects. Striatal volumes-of-interest (VOIs) uptake, VOIs asymmetry indices (AIs) and caudate/putamen (C/P) ratio were used as input for SVM individual classification using fivefold cross-validation.

Results

Univariate analyses showed significantly lower VOIs uptake, higher striatal AI and C/P ratio for each PS in comparison to controls (all p < 0.001). Among PS, higher degree of striatal impairment was observed in MSA-P and PSP, while CBS showed moderate uptake reduction and higher AI. Binary SVM classification showed 92.9% accuracy in distinguishing PS from controls. Classification based on each binary combination of PS ranged 62.9–83.7% accuracy with the most satisfactory results when separating CBS from the other PS. Sensitivity and specificity values were high and balanced ranging from 60 to 80% for all analyses with > 70% accuracy. Overall, striatal AI and C/P ratio on the more affected side had the highest weighting factors.

Conclusion

Semiquantitative 123I-FP-CIT SPECT striatal evaluation combined with SVM represents a promising approach to disentangle PD from non-degenerative conditions and from atypical PS at the early stage.
Literature
1.
go back to reference Fleury V, Brindel P, Nicastro N, Burkhard PR (2018) Descriptive epidemiology of parkinsonism in the Canton of Geneva, Switzerland. Parkinsonism Relat Disord 54:30–39CrossRefPubMed Fleury V, Brindel P, Nicastro N, Burkhard PR (2018) Descriptive epidemiology of parkinsonism in the Canton of Geneva, Switzerland. Parkinsonism Relat Disord 54:30–39CrossRefPubMed
2.
go back to reference Postuma RB, Berg B, Stern M, Poewe W, Olanow CW, Oertel W et al (2015) MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord 30:1591–1601CrossRefPubMed Postuma RB, Berg B, Stern M, Poewe W, Olanow CW, Oertel W et al (2015) MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord 30:1591–1601CrossRefPubMed
3.
go back to reference Rizzo G, Copetti M, Arcuti S, Martino D, Fontana A, Logroscino G (2016) Accuracy of clinical diagnosis of Parkinson disease: a systematic review and meta-analysis. Neurology 86(6):566–576CrossRefPubMed Rizzo G, Copetti M, Arcuti S, Martino D, Fontana A, Logroscino G (2016) Accuracy of clinical diagnosis of Parkinson disease: a systematic review and meta-analysis. Neurology 86(6):566–576CrossRefPubMed
4.
go back to reference Hoglinger GU, Respondek G, Stamelou M, Kurz C, Josephs KA, Lang AE et al (2017) Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord 32:853–864CrossRefPubMedPubMedCentral Hoglinger GU, Respondek G, Stamelou M, Kurz C, Josephs KA, Lang AE et al (2017) Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord 32:853–864CrossRefPubMedPubMedCentral
5.
go back to reference Armstrong MJ, Litvan I, Lang AE, Bak TH, Bhatia KP, Borroni B et al (2013) Criteria for the diagnosis of corticobasal degeneration. Neurology 80:496–503CrossRefPubMedPubMedCentral Armstrong MJ, Litvan I, Lang AE, Bak TH, Bhatia KP, Borroni B et al (2013) Criteria for the diagnosis of corticobasal degeneration. Neurology 80:496–503CrossRefPubMedPubMedCentral
6.
go back to reference Nicastro N, Garibotto V, Burkhard PR (2018) The role of molecular imaging in assessing degenerative parkinsonism—an updated review. Swiss Med Wkly 148:w14621PubMed Nicastro N, Garibotto V, Burkhard PR (2018) The role of molecular imaging in assessing degenerative parkinsonism—an updated review. Swiss Med Wkly 148:w14621PubMed
7.
go back to reference Tissingh G, Bergmans P, Booij J, Winogrodzka A, Stoof JC, Wolters EC, Van Royen EA (1997) [123I]beta-CIT single-photon emission tomography in Parkinson's disease reveals a smaller decline in dopamine transporters with age than in controls. Eur J Nucl Med 24:1171–1174PubMed Tissingh G, Bergmans P, Booij J, Winogrodzka A, Stoof JC, Wolters EC, Van Royen EA (1997) [123I]beta-CIT single-photon emission tomography in Parkinson's disease reveals a smaller decline in dopamine transporters with age than in controls. Eur J Nucl Med 24:1171–1174PubMed
8.
go back to reference Nicastro N, Garibotto V, Badoud S, Burkhard PR (2016) Scan without evidence of dopaminergic deficit: a 10-year retrospective study. Parkinsonism Relat Disord 31:53–58CrossRefPubMed Nicastro N, Garibotto V, Badoud S, Burkhard PR (2016) Scan without evidence of dopaminergic deficit: a 10-year retrospective study. Parkinsonism Relat Disord 31:53–58CrossRefPubMed
9.
go back to reference Nicastro N, Burkhard PR, Garibotto V (2018) Scan without evidence of dopaminergic deficit (SWEDD) in degenerative parkinsonism and dementia with Lewy bodies: a prospective study. J Neurol Sci 385:17–21CrossRefPubMed Nicastro N, Burkhard PR, Garibotto V (2018) Scan without evidence of dopaminergic deficit (SWEDD) in degenerative parkinsonism and dementia with Lewy bodies: a prospective study. J Neurol Sci 385:17–21CrossRefPubMed
10.
go back to reference 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 15:692–698CrossRefPubMed 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 15:692–698CrossRefPubMed
11.
go back to reference Vlaar AM, van Kroonenburgh MJ, Kessels AG, Weber WE (2007) Meta-analysis of the literature on diagnostic accuracy of SPECT in parkinsonian syndromes. BMC Neurol 7:27CrossRefPubMedPubMedCentral Vlaar AM, van Kroonenburgh MJ, Kessels AG, Weber WE (2007) Meta-analysis of the literature on diagnostic accuracy of SPECT in parkinsonian syndromes. BMC Neurol 7:27CrossRefPubMedPubMedCentral
12.
go back to reference Antonini A, Benti R, De Notaris R, Tesei S, Zecchinelli A, Sacilotto G, Meucci N, Canesi M, Mariani C, Pezzoli G, Gerundini P (2003) 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 24:149–150CrossRefPubMed Antonini A, Benti R, De Notaris R, Tesei S, Zecchinelli A, Sacilotto G, Meucci N, Canesi M, Mariani C, Pezzoli G, Gerundini P (2003) 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 24:149–150CrossRefPubMed
13.
go back to reference Cilia R, Rossi C, Frosini D, Volterrani D, Siri C, Pagni C, Benti R, Pezzoli G, Bonuccelli U, Antonini A, Ceravolo R (2011) Dopamine transporter SPECT imaging in corticobasal syndrome. PLoS One 6:e18301CrossRefPubMedPubMedCentral Cilia R, Rossi C, Frosini D, Volterrani D, Siri C, Pagni C, Benti R, Pezzoli G, Bonuccelli U, Antonini A, Ceravolo R (2011) Dopamine transporter SPECT imaging in corticobasal syndrome. PLoS One 6:e18301CrossRefPubMedPubMedCentral
14.
go back to reference O'Sullivan SS, Burn DJ, Holton JL, Lees AJ (2008) Normal dopamine transporter single photon-emission CT scan in corticobasal degeneration. Mov Disord 23:2424–2426CrossRefPubMed O'Sullivan SS, Burn DJ, Holton JL, Lees AJ (2008) Normal dopamine transporter single photon-emission CT scan in corticobasal degeneration. Mov Disord 23:2424–2426CrossRefPubMed
16.
go back to reference Kloppel S, Abdulkadir A, Jack CR Jr, Koutsouleris N, Mourao-Miranda J, Vemuri P (2012) Diagnostic neuroimaging across diseases. Neuroimage 61:457–463CrossRefPubMed Kloppel S, Abdulkadir A, Jack CR Jr, Koutsouleris N, Mourao-Miranda J, Vemuri P (2012) Diagnostic neuroimaging across diseases. Neuroimage 61:457–463CrossRefPubMed
17.
go back to reference Huppertz HJ, Moller L, Sudmeyer M, Hilker R, Hattingen E, Egger K et al (2016) Differentiation of neurodegenerative parkinsonian syndromes by volumetric magnetic resonance imaging analysis and support vector machine classification. Mov Disord 31:1506–1517CrossRefPubMed Huppertz HJ, Moller L, Sudmeyer M, Hilker R, Hattingen E, Egger K et al (2016) Differentiation of neurodegenerative parkinsonian syndromes by volumetric magnetic resonance imaging analysis and support vector machine classification. Mov Disord 31:1506–1517CrossRefPubMed
18.
go back to reference Segovia F, Illan IA, Gorriz JM, Ramirez J, Rominger A, Levin J (2015) Distinguishing Parkinson's disease from atypical parkinsonian syndromes using PET data and a computer system based on support vector machines and Bayesian networks. Front Comput Neurosci 9:137CrossRefPubMedPubMedCentral Segovia F, Illan IA, Gorriz JM, Ramirez J, Rominger A, Levin J (2015) Distinguishing Parkinson's disease from atypical parkinsonian syndromes using PET data and a computer system based on support vector machines and Bayesian networks. Front Comput Neurosci 9:137CrossRefPubMedPubMedCentral
19.
go back to reference Castillo-Barnes D, Ramirez J, Segovia F, Martinez-Murcia FJ, Salas-Gonzalez D, Gorriz JM (2018) Robust ensemble classification methodology for I123-Ioflupane SPECT images and multiple heterogeneous biomarkers in the diagnosis of Parkinson's disease. Front Neuroinform 12:53CrossRefPubMedPubMedCentral Castillo-Barnes D, Ramirez J, Segovia F, Martinez-Murcia FJ, Salas-Gonzalez D, Gorriz JM (2018) Robust ensemble classification methodology for I123-Ioflupane SPECT images and multiple heterogeneous biomarkers in the diagnosis of Parkinson's disease. Front Neuroinform 12:53CrossRefPubMedPubMedCentral
20.
go back to reference Cherubini A, Morelli M, Nistico R, Salsone M, Arabia G, Vasta R, Augimeri A, Caligiuri ME, Quattrone A (2014) Magnetic resonance support vector machine discriminates between Parkinson disease and progressive supranuclear palsy. Mov Disord 29:266–269CrossRefPubMed Cherubini A, Morelli M, Nistico R, Salsone M, Arabia G, Vasta R, Augimeri A, Caligiuri ME, Quattrone A (2014) Magnetic resonance support vector machine discriminates between Parkinson disease and progressive supranuclear palsy. Mov Disord 29:266–269CrossRefPubMed
21.
go back to reference Haller S, Badoud S, Nguyen D, Garibotto V, Lovblad KO, Burkhard PR (2012) Individual detection of patients with Parkinson disease using support vector machine analysis of diffusion tensor imaging data: initial results. Am J Neuroradiol 33:2123–2128CrossRefPubMedPubMedCentral Haller S, Badoud S, Nguyen D, Garibotto V, Lovblad KO, Burkhard PR (2012) Individual detection of patients with Parkinson disease using support vector machine analysis of diffusion tensor imaging data: initial results. Am J Neuroradiol 33:2123–2128CrossRefPubMedPubMedCentral
22.
go back to reference Focke NK, Helms G, Scheewe S, Pantel PM, Bachmann CG, Dechent P et al (2011) Individual voxel-based subtype prediction can differentiate progressive supranuclear palsy from idiopathic Parkinson syndrome and healthy controls. Hum Brain Mapp 32:1905–1915CrossRefPubMedPubMedCentral Focke NK, Helms G, Scheewe S, Pantel PM, Bachmann CG, Dechent P et al (2011) Individual voxel-based subtype prediction can differentiate progressive supranuclear palsy from idiopathic Parkinson syndrome and healthy controls. Hum Brain Mapp 32:1905–1915CrossRefPubMedPubMedCentral
23.
go back to reference Augimeri A, Cherubini A, Cascini GL, Galea D, Caligiuri ME, Barbagallo G, Arabia G, Quattrone A (2016) CADA-computer-aided DATSCAN analysis. EJNMMI Phys 3(1):4CrossRefPubMedPubMedCentral Augimeri A, Cherubini A, Cascini GL, Galea D, Caligiuri ME, Barbagallo G, Arabia G, Quattrone A (2016) CADA-computer-aided DATSCAN analysis. EJNMMI Phys 3(1):4CrossRefPubMedPubMedCentral
24.
go back to reference Martinez-Murcia F, Górriz J, Ramírez J, Illan IA, Ortiz A (2014) Automatic detection of Parkinsonism using significance measures and component analysis in datscan imaging. Neurocomputing 126(Suppl. C):58–70CrossRef Martinez-Murcia F, Górriz J, Ramírez J, Illan IA, Ortiz A (2014) Automatic detection of Parkinsonism using significance measures and component analysis in datscan imaging. Neurocomputing 126(Suppl. C):58–70CrossRef
25.
go back to reference Segovia F, Górriz JM, Ramírez J, Martinez-Murcia FJ, Levin J, Schuberth M et al (2017) Multivariate analysis of 18F-DMFP pet data to assist the diagnosis of Parkinsonism. Front Neuroinform 11:23CrossRefPubMedPubMedCentral Segovia F, Górriz JM, Ramírez J, Martinez-Murcia FJ, Levin J, Schuberth M et al (2017) Multivariate analysis of 18F-DMFP pet data to assist the diagnosis of Parkinsonism. Front Neuroinform 11:23CrossRefPubMedPubMedCentral
26.
go back to reference Badoud S, Van De Ville D, Nicastro N, Garibotto V, Burkhard PR, Haller S (2016) Discriminating among degenerative parkinsonisms using advanced (123)I-ioflupane SPECT analyses. Neuroimage Clin 12:234–240CrossRefPubMedPubMedCentral Badoud S, Van De Ville D, Nicastro N, Garibotto V, Burkhard PR, Haller S (2016) Discriminating among degenerative parkinsonisms using advanced (123)I-ioflupane SPECT analyses. Neuroimage Clin 12:234–240CrossRefPubMedPubMedCentral
27.
go back to reference Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ et al (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676CrossRefPubMedPubMedCentral Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ et al (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676CrossRefPubMedPubMedCentral
28.
go back to reference Nicastro N, Garibotto V, Poncet A, Badoud S, Burkhard PR (2016) Establishing on-site reference values for (123)I-FP-CIT SPECT (DaTSCAN(R)) using a cohort of individuals with non-degenerative conditions. Mol Imaging Biol 18:302–312CrossRefPubMed Nicastro N, Garibotto V, Poncet A, Badoud S, Burkhard PR (2016) Establishing on-site reference values for (123)I-FP-CIT SPECT (DaTSCAN(R)) using a cohort of individuals with non-degenerative conditions. Mol Imaging Biol 18:302–312CrossRefPubMed
29.
go back to reference Radau PE, Slomka PJ, Julin P, Svensson L, Wahlund LO (2001) Evaluation of linear registration algorithms for brain SPECT and the errors due to hypoperfusion lesions. Med Phys 28:1660–1668CrossRefPubMed Radau PE, Slomka PJ, Julin P, Svensson L, Wahlund LO (2001) Evaluation of linear registration algorithms for brain SPECT and the errors due to hypoperfusion lesions. Med Phys 28:1660–1668CrossRefPubMed
30.
go back to reference Lunardon N, Menardi G, Torelli N (2014) Rose—a package for binary imbalanced learning. R J 6:79–89CrossRef Lunardon N, Menardi G, Torelli N (2014) Rose—a package for binary imbalanced learning. R J 6:79–89CrossRef
31.
go back to reference Kohavi R (1995) A study of cross-validation and bootstrap for accuracy estimation and model selection. In: Proceedings of the 14th international joint conference on artificial intelligence vol 2, pp 1137–1145 Kohavi R (1995) A study of cross-validation and bootstrap for accuracy estimation and model selection. In: Proceedings of the 14th international joint conference on artificial intelligence vol 2, pp 1137–1145
32.
go back to reference Nicastro N, Garibotto V, Burkhard PR (2018) 123I-FP-CIT SPECT accurately distinguishes parkinsonian from cerebellar variant of multiple system atrophy. Clin Nucl Med 43:e33–e36CrossRefPubMed Nicastro N, Garibotto V, Burkhard PR (2018) 123I-FP-CIT SPECT accurately distinguishes parkinsonian from cerebellar variant of multiple system atrophy. Clin Nucl Med 43:e33–e36CrossRefPubMed
33.
go back to reference Skanjeti A, Castellano G, Elia BO, Zotta M, Dazzara F, Manfredi M, Galati A, Grimaldi S, Balma M, Pellerito RE, Podio V (2015) Multicenter semiquantitative evaluation of (123)I-FP-CIT brain SPECT. J Neuroimaging 25:1023–1029CrossRefPubMed Skanjeti A, Castellano G, Elia BO, Zotta M, Dazzara F, Manfredi M, Galati A, Grimaldi S, Balma M, Pellerito RE, Podio V (2015) Multicenter semiquantitative evaluation of (123)I-FP-CIT brain SPECT. J Neuroimaging 25:1023–1029CrossRefPubMed
34.
go back to reference Pirker W, Asenbaum S, Bencsits G, Prayer D, Gerschlager W, Deecke L, Brücke T (2000) [123I]beta-CIT SPECT in multiple system atrophy, progressive supranuclear palsy, and corticobasal degeneration. Mov Disord 15:1158–1167CrossRefPubMed Pirker W, Asenbaum S, Bencsits G, Prayer D, Gerschlager W, Deecke L, Brücke T (2000) [123I]beta-CIT SPECT in multiple system atrophy, progressive supranuclear palsy, and corticobasal degeneration. Mov Disord 15:1158–1167CrossRefPubMed
35.
go back to reference Filippi L, Manni C, Pierantozzi M, Brusa L, Danieli R, Stanzione P, Schillaci O (2006) 123I-FP-CIT in progressive supranuclear palsy and in Parkinson's disease: a SPECT semiquantitative study. Nucl Med Commun 27:381–386CrossRefPubMed Filippi L, Manni C, Pierantozzi M, Brusa L, Danieli R, Stanzione P, Schillaci O (2006) 123I-FP-CIT in progressive supranuclear palsy and in Parkinson's disease: a SPECT semiquantitative study. Nucl Med Commun 27:381–386CrossRefPubMed
36.
go back to reference Oliveira FP, Castelo-Branco M (2015) Computer-aided diagnosis of Parkinson's disease based on [(123)I]FP-CIT SPECT binding potential images, using the voxels-as-features approach and support vector machines. J Neural Eng 12:026008CrossRefPubMed Oliveira FP, Castelo-Branco M (2015) Computer-aided diagnosis of Parkinson's disease based on [(123)I]FP-CIT SPECT binding potential images, using the voxels-as-features approach and support vector machines. J Neural Eng 12:026008CrossRefPubMed
Metadata
Title
Classification of degenerative parkinsonism subtypes by support-vector-machine analysis and striatal 123I-FP-CIT indices
Authors
Nicolas Nicastro
Jennifer Wegrzyk
Maria Giulia Preti
Vanessa Fleury
Dimitri Van de Ville
Valentina Garibotto
Pierre R. Burkhard
Publication date
01-07-2019
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 7/2019
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-019-09330-z

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