Skip to main content
Top
Published in: Clinical Neuroradiology 4/2019

01-12-2019 | Original Article

Improved Automatic Morphology-Based Classification of Parkinson’s Disease and Progressive Supranuclear Palsy

Authors: Aron S. Talai, Zahinoor Ismail, Jan Sedlacik, Kai Boelmans, Nils D. Forkert

Published in: Clinical Neuroradiology | Issue 4/2019

Login to get access

Abstract

Objectives

The overlapping symptoms of Parkinson’s disease (PD) and progressive supranuclear palsy—Richardson’s syndrome (PSP-RS) often make a correct clinical diagnosis difficult. The volume of subcortical brain structures derived from high-resolution T1-weighted magnetic resonance imaging (MRI) datasets is frequently used for individual level classification of PD and PSP-RS patients. The aim of this study was to evaluate the benefit of including additional morphological features beyond the simple regional volume, as well as clinical features, and morphological features of cortical structures for an automatic classification of PD and PSP-RS patients.

Material and Methods

A total of 98 high-resolution T1-weighted MRI datasets from 76 PD patients, and 22 PSP-RS patients were available for this study. Using an atlas-based approach, the volume, surface area, and surface-area-to-volume ratio (SA:V) of 21 subcortical and 48 cortical brain regions were calculated and used as features for a support vector machine classification after application of a RELIEF feature selection method.

Results

The comparison of the classification results suggests that including all three morphological parameters (volume, surface area and SA:V) can considerably improve classification accuracy compared to using volume or surface area alone. Likewise, including clinical patient features in addition to morphological parameters also considerably increases the classification accuracy. In contrast to this, integrating morphological features of other cortical structures did not lead to improved classification accuracy. Using this optimal set-up, an accuracy of 98% was achieved with only one falsely classified PD and one falsely classified PSP-RS patient.

Conclusion

The results of this study suggest that clinical features as well as more advanced morphological features should be used for future computer-aided diagnosis systems to differentiate PD and PSP-RS patients based on morphological parameters.
Literature
1.
go back to reference Tolosa E, Wenning G, Poewe W. The diagnosis of Parkinson’s disease. Lancet Neurol. 2006;5:75–86.PubMed Tolosa E, Wenning G, Poewe W. The diagnosis of Parkinson’s disease. Lancet Neurol. 2006;5:75–86.PubMed
2.
go back to reference Olanow CW, Hauser RA, Jankovic J, Langston W, Lang A, Poewe W, Tolosa E, Stocchi F, Melamed E, Eyal E, Rascol O. A randomized, double-blind, placebo-controlled, delayed start study to assess rasagiline as a disease modifying therapy in Parkinson’s disease (the ADAGIO study): rationale, design, and baseline characteristics. Mov Disord. 2008;23:2194–201.PubMed Olanow CW, Hauser RA, Jankovic J, Langston W, Lang A, Poewe W, Tolosa E, Stocchi F, Melamed E, Eyal E, Rascol O. A randomized, double-blind, placebo-controlled, delayed start study to assess rasagiline as a disease modifying therapy in Parkinson’s disease (the ADAGIO study): rationale, design, and baseline characteristics. Mov Disord. 2008;23:2194–201.PubMed
3.
go back to reference Pellicano C, Assogna F, Cellupica N, Piras F, Pierantozzi M, Stefani A, Cerroni R, Mercuri B, Caltagirone C, Pontieri FE, Spalletta G. Neuropsychiatric and cognitive profile of early Richardson’s syndrome, progressive supranuclear Palsy-parkinsonism and Parkinson’s disease. Parkinsonism Relat Disord. 2017;45:50–6.PubMed Pellicano C, Assogna F, Cellupica N, Piras F, Pierantozzi M, Stefani A, Cerroni R, Mercuri B, Caltagirone C, Pontieri FE, Spalletta G. Neuropsychiatric and cognitive profile of early Richardson’s syndrome, progressive supranuclear Palsy-parkinsonism and Parkinson’s disease. Parkinsonism Relat Disord. 2017;45:50–6.PubMed
4.
go back to reference Hughes AJ, Daniel SE, Ben-Shlomo Y, Lees AJ. The accuracy of diagnosis of parkinsonian syndromes in a specialist movement disorder service. Brain. 2002;125:861–70.PubMed Hughes AJ, Daniel SE, Ben-Shlomo Y, Lees AJ. The accuracy of diagnosis of parkinsonian syndromes in a specialist movement disorder service. Brain. 2002;125:861–70.PubMed
5.
go back to reference Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, Goetz CG, Golbe LI, Grafman J, Growdon JH, Hallett M, Jankovic J, Quinn NP, Tolosa E, Zee DS. 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, Goetz CG, Golbe LI, Grafman J, Growdon JH, Hallett M, Jankovic J, Quinn NP, Tolosa E, Zee DS. 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
6.
go back to reference Bensimon G, Ludolph A, Agid Y, Vidailhet M, Payan C, Leigh PN; NNIPPS Study Group. Riluzole treatment, survival and diagnostic criteria in Parkinson plus disorders: the NNIPPS study. Brain. 2009;132:156–71.PubMed Bensimon G, Ludolph A, Agid Y, Vidailhet M, Payan C, Leigh PN; NNIPPS Study Group. Riluzole treatment, survival and diagnostic criteria in Parkinson plus disorders: the NNIPPS study. Brain. 2009;132:156–71.PubMed
7.
go back to reference Davie CA. A review of Parkinson’s disease. Br Med Bull. 2008;86:109–27.PubMed Davie CA. A review of Parkinson’s disease. Br Med Bull. 2008;86:109–27.PubMed
8.
go back to reference Marx S, Respondek G, Stamelou M, Dowiasch S, Stoll J, Bremmer F, Oertel WH, Höglinger GU, Einhäuser W. Validation of mobile eye-tracking as novel and efficient means for differentiating progressive supranuclear palsy from Parkinson’s disease. Front Behav Neurosci. 2012;6:1–11. Marx S, Respondek G, Stamelou M, Dowiasch S, Stoll J, Bremmer F, Oertel WH, Höglinger GU, Einhäuser W. Validation of mobile eye-tracking as novel and efficient means for differentiating progressive supranuclear palsy from Parkinson’s disease. Front Behav Neurosci. 2012;6:1–11.
9.
go back to reference Egerton T, Williams DR, Iansek R. Comparison of gait in progressive supranuclear palsy, Parkinson’s disease and healthy older adults. BMC Neurol. 2012;12:116.PubMedPubMedCentral Egerton T, Williams DR, Iansek R. Comparison of gait in progressive supranuclear palsy, Parkinson’s disease and healthy older adults. BMC Neurol. 2012;12:116.PubMedPubMedCentral
10.
go back to reference Tang CC, Poston KL, Eckert T, Feigin A, Frucht S, Gudesblatt M, Dhawan V, Lesser M, Vonsattel JP, Fahn S, Eidelberg D. Differential diagnosis of parkinsonism: a metabolic imaging study using pattern analysis. Lancet Neurol. 2010;9:149–58.PubMedPubMedCentral Tang CC, Poston KL, Eckert T, Feigin A, Frucht S, Gudesblatt M, Dhawan V, Lesser M, Vonsattel JP, Fahn S, Eidelberg D. Differential diagnosis of parkinsonism: a metabolic imaging study using pattern analysis. Lancet Neurol. 2010;9:149–58.PubMedPubMedCentral
11.
go back to reference Eckert T, Sailer M, Kaufmann J, Schrader C, Peschel T, Bodammer N, Heinze HJ, Schoenfeld MA. Differentiation of idiopathic Parkinson’s disease, multiple system atrophy, progressive supranuclear palsy, and healthy controls using magnetization transfer imaging. Neuroimage. 2004;21:229–35.PubMed Eckert T, Sailer M, Kaufmann J, Schrader C, Peschel T, Bodammer N, Heinze HJ, Schoenfeld MA. Differentiation of idiopathic Parkinson’s disease, multiple system atrophy, progressive supranuclear palsy, and healthy controls using magnetization transfer imaging. Neuroimage. 2004;21:229–35.PubMed
12.
go back to reference Forkert ND, Schmidt-Richberg A, Treszl A, Hilgetag C, Fiehler J, Münchau A, Handels H, Boelmans K. Automated volumes-of-interest identification for classical and atypical parkinsonian syndrome differentiation using T2’ MR imaging. Methods Inf Med. 2013;52:128–36.PubMed Forkert ND, Schmidt-Richberg A, Treszl A, Hilgetag C, Fiehler J, Münchau A, Handels H, Boelmans K. Automated volumes-of-interest identification for classical and atypical parkinsonian syndrome differentiation using T2’ MR imaging. Methods Inf Med. 2013;52:128–36.PubMed
13.
go back to reference Duchesne S, Rolland Y, Verin M. Automated computer differential classification in parkinsonian syndromes via pattern analysis on MRI. Acad Radiol. 2009;16:61–70.PubMed Duchesne S, Rolland Y, Verin M. Automated computer differential classification in parkinsonian syndromes via pattern analysis on MRI. Acad Radiol. 2009;16:61–70.PubMed
14.
go back to reference Quattrone A, Nicoletti G, Messina D, Fera F, Condino F, Pugliese P, Lanza P, Barone P, Morgante L, Zappia M, Aguglia U, Gallo O. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214–21.PubMed Quattrone A, Nicoletti G, Messina D, Fera F, Condino F, Pugliese P, Lanza P, Barone P, Morgante L, Zappia M, Aguglia U, Gallo O. MR imaging index for differentiation of progressive supranuclear palsy from Parkinson disease and the Parkinson variant of multiple system atrophy. Radiology. 2008;246:214–21.PubMed
15.
go back to reference Messina D, Cerasa A, Condino F, Arabia G, Novellino F, Nicoletti G, Salsone M, Morelli M, Lanza PL, Quattrone A. Patterns of brain atrophy in Parkinson’s disease, progressive supranuclear palsy and multiple system atrophy. Parkinsonism Relat Disord. 2011;17:172–6.PubMed Messina D, Cerasa A, Condino F, Arabia G, Novellino F, Nicoletti G, Salsone M, Morelli M, Lanza PL, Quattrone A. Patterns of brain atrophy in Parkinson’s disease, progressive supranuclear palsy and multiple system atrophy. Parkinsonism Relat Disord. 2011;17:172–6.PubMed
16.
go back to reference Focke NK, Helms G, Scheewe S, Pantel PM, Bachmann CG, Dechent P, Ebentheuer J, Mohr A, Paulus W, Trenkwalder C. Individual voxel-based subtype prediction can differentiate progressive supranuclear palsy from idiopathic Parkinson syndrome and healthy controls. Hum Brain Mapp. 2011;32:1905–15.PubMed Focke NK, Helms G, Scheewe S, Pantel PM, Bachmann CG, Dechent P, Ebentheuer J, Mohr A, Paulus W, Trenkwalder C. Individual voxel-based subtype prediction can differentiate progressive supranuclear palsy from idiopathic Parkinson syndrome and healthy controls. Hum Brain Mapp. 2011;32:1905–15.PubMed
17.
go back to reference Gama RL, Távora DF, Bomfim RC, Silva CE, Bruin VM, Bruin PF. Morphometry MRI in the differential diagnosis of parkinsonian syndromes. Arq Neuropsiquiatr. 2010;68:333–8.PubMed Gama RL, Távora DF, Bomfim RC, Silva CE, Bruin VM, Bruin PF. Morphometry MRI in the differential diagnosis of parkinsonian syndromes. Arq Neuropsiquiatr. 2010;68:333–8.PubMed
18.
go back to reference Price S, Paviour D, Scahill R, Stevens J, Rossor M, Lees A, Fox N. Voxel-based morphometry detects patterns of atrophy that help differentiate progressive supranuclear palsy and Parkinson’s disease. Neuroimage. 2004;23:663–9.PubMed Price S, Paviour D, Scahill R, Stevens J, Rossor M, Lees A, Fox N. Voxel-based morphometry detects patterns of atrophy that help differentiate progressive supranuclear palsy and Parkinson’s disease. Neuroimage. 2004;23:663–9.PubMed
19.
go back to reference Scherfler C, Göbel G, Müller C, Nocker M, Wenning GK, Schocke M, Poewe W, Seppi K. Diagnostic potential of automated subcortical volume segmentation in atypical parkinsonism. Neurology. 2016;86:1242–9.PubMed Scherfler C, Göbel G, Müller C, Nocker M, Wenning GK, Schocke M, Poewe W, Seppi K. Diagnostic potential of automated subcortical volume segmentation in atypical parkinsonism. Neurology. 2016;86:1242–9.PubMed
20.
go back to reference Sarica A, Critelli C, Guzzi PH, Cerasa A, Quattrone A, Cannataro M. Application of different classification techniques on brain morphological data. Comput Med Syst (CBMS), 2013 IEEE 26th Int Symp on IEEE. 2013. pp. 425–8. Sarica A, Critelli C, Guzzi PH, Cerasa A, Quattrone A, Cannataro M. Application of different classification techniques on brain morphological data. Comput Med Syst (CBMS), 2013 IEEE 26th Int Symp on IEEE. 2013. pp. 425–8.
21.
go back to reference Lee JH, Han YH, Kang BM, Mun CW, Lee SJ, Baik SK. Quantitative assessment of subcortical atrophy and iron content in progressive supranuclear palsy and parkinsonian variant of multiple system atrophy. J Neurol. 2013;260:2094–101.PubMed Lee JH, Han YH, Kang BM, Mun CW, Lee SJ, Baik SK. Quantitative assessment of subcortical atrophy and iron content in progressive supranuclear palsy and parkinsonian variant of multiple system atrophy. J Neurol. 2013;260:2094–101.PubMed
22.
go back to reference Sakurai K, Tokumaru AM, Shimoji K, Murayama S, Kanemaru K, Morimoto S, Aiba I, Nakagawa M, Ozawa Y, Shimohira M, Matsukawa N, Hashizume Y, Shibamoto Y. Beyond the midbrain atrophy: wide spectrum of structural MRI finding in cases of pathologically proven progressive supranuclear palsy. Neuroradiology. 2017;59:431–43.PubMed Sakurai K, Tokumaru AM, Shimoji K, Murayama S, Kanemaru K, Morimoto S, Aiba I, Nakagawa M, Ozawa Y, Shimohira M, Matsukawa N, Hashizume Y, Shibamoto Y. Beyond the midbrain atrophy: wide spectrum of structural MRI finding in cases of pathologically proven progressive supranuclear palsy. Neuroradiology. 2017;59:431–43.PubMed
23.
go back to reference Dotson VM, Szymkowicz SM, Sozda CN, Kirton JW, Green ML, O’Shea A, McLaren ME, Anton SD, Manini TM, Woods AJ. Age differences in prefrontal surface area and thickness in middle aged to older adults. Front Aging Neurosci. 2016;7:1–9. Dotson VM, Szymkowicz SM, Sozda CN, Kirton JW, Green ML, O’Shea A, McLaren ME, Anton SD, Manini TM, Woods AJ. Age differences in prefrontal surface area and thickness in middle aged to older adults. Front Aging Neurosci. 2016;7:1–9.
24.
go back to reference Jubault T, Gagnon JF, Karama S, Ptito A, Lafontaine AL, Evans AC, Monchi O. Patterns of cortical thickness and surface area in early Parkinson’s disease. Neuroimage. 2011;55:462–7.PubMed Jubault T, Gagnon JF, Karama S, Ptito A, Lafontaine AL, Evans AC, Monchi O. Patterns of cortical thickness and surface area in early Parkinson’s disease. Neuroimage. 2011;55:462–7.PubMed
25.
go back to reference Gerrits NJ, van Loenhoud AC, van den Berg SF, Berendse HW, Foncke EM, Klein M, Stoffers D, van der Werf YD, van den Heuvel OA. Cortical thickness, surface area and subcortical volume differentially contribute to cognitive heterogeneity in Parkinson’s disease. PLoS ONE. 2016;11:1–14. Gerrits NJ, van Loenhoud AC, van den Berg SF, Berendse HW, Foncke EM, Klein M, Stoffers D, van der Werf YD, van den Heuvel OA. Cortical thickness, surface area and subcortical volume differentially contribute to cognitive heterogeneity in Parkinson’s disease. PLoS ONE. 2016;11:1–14.
26.
go back to reference Dickerson BC, Feczko E, Augustinack JC, Pacheco J, Morris JC, Fischl B, Buckner RL. Differential effects of aging and Alzheimer’s disease on medial temporal lobe cortical thickness and surface area. Neurobiol Aging. 2009;30:432–40.PubMed Dickerson BC, Feczko E, Augustinack JC, Pacheco J, Morris JC, Fischl B, Buckner RL. Differential effects of aging and Alzheimer’s disease on medial temporal lobe cortical thickness and surface area. Neurobiol Aging. 2009;30:432–40.PubMed
27.
go back to reference Worker A, Blain C, Jarosz J, Chaudhuri KR, Barker GJ, Williams SC, Brown R, Leigh PN, Simmons A. Cortical thickness, surface area and volume measures in Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy. PLoS ONE. 2014;9:1–15. Worker A, Blain C, Jarosz J, Chaudhuri KR, Barker GJ, Williams SC, Brown R, Leigh PN, Simmons A. Cortical thickness, surface area and volume measures in Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy. PLoS ONE. 2014;9:1–15.
28.
go back to reference Planetta PJ, Ofori E, Pasternak O, Burciu RG, Shukla P, DeSimone JC, Okun MS, McFarland NR, Vaillancourt DE. Free-water imaging in Parkinson’s disease and atypical parkinsonism. Brain. 2016;139:495–508.PubMed Planetta PJ, Ofori E, Pasternak O, Burciu RG, Shukla P, DeSimone JC, Okun MS, McFarland NR, Vaillancourt DE. Free-water imaging in Parkinson’s disease and atypical parkinsonism. Brain. 2016;139:495–508.PubMed
29.
go back to reference Hirschauer TJ, Adeli H, Buford JA. Computer-aided diagnosis of Parkinson’s disease using enhanced probabilistic neural network. J Med Syst. 2015;39:179.PubMed Hirschauer TJ, Adeli H, Buford JA. Computer-aided diagnosis of Parkinson’s disease using enhanced probabilistic neural network. J Med Syst. 2015;39:179.PubMed
30.
go back to reference Long D, Wang J, Xuan M, Gu Q, Xu X, Kong D, Zhang M. Automatic classification of early Parkinson’s disease with multi-modal MR imaging. PLoS ONE. 2012;7:1–9. Long D, Wang J, Xuan M, Gu Q, Xu X, Kong D, Zhang M. Automatic classification of early Parkinson’s disease with multi-modal MR imaging. PLoS ONE. 2012;7:1–9.
31.
go back to reference Péran P, Cherubini A, Assogna F, Piras F, Quattrocchi C, Peppe A, Celsis P, Rascol O, Démonet JF, Stefani A, Pierantozzi M, Pontieri FE, Caltagirone C, Spalletta G, Sabatini U. Magnetic resonance imaging markers of Parkinson’s disease nigrostriatal signature. Brain. 2010;133:3423–33.PubMed Péran P, Cherubini A, Assogna F, Piras F, Quattrocchi C, Peppe A, Celsis P, Rascol O, Démonet JF, Stefani A, Pierantozzi M, Pontieri FE, Caltagirone C, Spalletta G, Sabatini U. Magnetic resonance imaging markers of Parkinson’s disease nigrostriatal signature. Brain. 2010;133:3423–33.PubMed
32.
go back to reference Morisi R, Cha M, Arafa M, Zagrouba E. Binary and multi-class parkinsonian disorders classification using support vector machines. In: Lecture notes in computer science. 2015. pp. 379–86. Morisi R, Cha M, Arafa M, Zagrouba E. Binary and multi-class parkinsonian disorders classification using support vector machines. In: Lecture notes in computer science. 2015. pp. 379–86.
33.
go back to reference Ota M, Nakata Y, Ito K, Kamiya K, Ogawa M, Murata M, Obu S, Kunugi H, Sato N. Differential diagnosis tool for parkinsonian syndrome using multiple structural brain measures. Comput Math Methods Med. 2013;2013:571289.PubMedPubMedCentral Ota M, Nakata Y, Ito K, Kamiya K, Ogawa M, Murata M, Obu S, Kunugi H, Sato N. Differential diagnosis tool for parkinsonian syndrome using multiple structural brain measures. Comput Math Methods Med. 2013;2013:571289.PubMedPubMedCentral
34.
go back to reference Segovia F, Illán IA, Górriz JM, Ramírez J, Rominger A, Levin J. 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. 2015;9:1–8. Segovia F, Illán IA, Górriz JM, Ramírez J, Rominger A, Levin J. 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. 2015;9:1–8.
35.
go back to reference Prashanth R, Dutta Roy S, Mandal PK, Ghosh S. High-accuracy detection of early Parkinson’s disease through multimodal features and machine learning. Int J Med Inform. 2016;90:13–21.PubMed Prashanth R, Dutta Roy S, Mandal PK, Ghosh S. High-accuracy detection of early Parkinson’s disease through multimodal features and machine learning. Int J Med Inform. 2016;90:13–21.PubMed
36.
go back to reference Boelmans K, Holst B, Hackius M, Finsterbusch J, Gerloff C, Fiehler J, Münchau A. Brain iron deposition fingerprints in Parkinson’s disease and progressive supranuclear palsy. Mov Disord. 2012;27:421–7.PubMed Boelmans K, Holst B, Hackius M, Finsterbusch J, Gerloff C, Fiehler J, Münchau A. Brain iron deposition fingerprints in Parkinson’s disease and progressive supranuclear palsy. Mov Disord. 2012;27:421–7.PubMed
37.
go back to reference Fellner F, Holl K, Held P, Fellner C, Schmitt R, Böhm-Jurkovic H. A T1-weighted rapid three-dimensional gradient-echo technique (MP-RAGE) in preoperative MRI of intracranial tumours. Neuroradiology. 1996;38:199–206.PubMed Fellner F, Holl K, Held P, Fellner C, Schmitt R, Böhm-Jurkovic H. A T1-weighted rapid three-dimensional gradient-echo technique (MP-RAGE) in preoperative MRI of intracranial tumours. Neuroradiology. 1996;38:199–206.PubMed
38.
go back to reference Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, Paus T, Simpson G, Pike B, Holmes C, Collins L, Thompson P, MacDonald D, Iacoboni M, Schormann T, Amunts K, Palomero-Gallagher N, Geyer S, Parsons L, Narr K, Kabani N, Le Goualher G, Boomsma D, Cannon T, Kawashima R, Mazoyer B. A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond, B, Biol Sci. 2001;356:1293–322.PubMedPubMedCentral Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, Paus T, Simpson G, Pike B, Holmes C, Collins L, Thompson P, MacDonald D, Iacoboni M, Schormann T, Amunts K, Palomero-Gallagher N, Geyer S, Parsons L, Narr K, Kabani N, Le Goualher G, Boomsma D, Cannon T, Kawashima R, Mazoyer B. A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond, B, Biol Sci. 2001;356:1293–322.PubMedPubMedCentral
39.
go back to reference Ourselin S, Roche A, Subsol G, Pennec X, Ayache N. Reconstructing a 3D structure from serial histological sections. Image Vis Comput. 2001;19:25–31. Ourselin S, Roche A, Subsol G, Pennec X, Ayache N. Reconstructing a 3D structure from serial histological sections. Image Vis Comput. 2001;19:25–31.
40.
go back to reference Modat M, Ridgway GR, Taylor ZA, Lehmann M, Barnes J, Hawkes DJ, Fox NC, Ourselin S. Fast free-form deformation using graphics processing units. Comput Methods Programs Biomed. 2010;98:278–84.PubMed Modat M, Ridgway GR, Taylor ZA, Lehmann M, Barnes J, Hawkes DJ, Fox NC, Ourselin S. Fast free-form deformation using graphics processing units. Comput Methods Programs Biomed. 2010;98:278–84.PubMed
41.
go back to reference Kononenko I, Šimec E, Robnik-Šikonja M. Overcoming the myopia of inductive learning algorithms with RELIEFF. Appl Intell. 1997;7:39–55. Kononenko I, Šimec E, Robnik-Šikonja M. Overcoming the myopia of inductive learning algorithms with RELIEFF. Appl Intell. 1997;7:39–55.
42.
go back to reference Chang C, Lin C. LIBSVM: A Library for Support Vector Machines. ACM Trans Intell Syst Technol. 2011;2:27:1-27. Chang C, Lin C. LIBSVM: A Library for Support Vector Machines. ACM Trans Intell Syst Technol. 2011;2:27:1-27.
43.
go back to reference Du G, Lewis MM, Kanekar S, Sterling NW, He L, Kong L, Li R, Huang X. Combined diffusion tensor imaging and apparent transverse relaxation rate differentiate Parkinson disease and atypical parkinsonism. AJNR Am J Neuroradiol. 2017;38:966–72.PubMedPubMedCentral Du G, Lewis MM, Kanekar S, Sterling NW, He L, Kong L, Li R, Huang X. Combined diffusion tensor imaging and apparent transverse relaxation rate differentiate Parkinson disease and atypical parkinsonism. AJNR Am J Neuroradiol. 2017;38:966–72.PubMedPubMedCentral
44.
go back to reference Dubois B, Pillon B. Cognitive deficits in Parkinson’s disease. J Neurol. 1996;244:2–8. Dubois B, Pillon B. Cognitive deficits in Parkinson’s disease. J Neurol. 1996;244:2–8.
45.
go back to reference Salvatore C, Cerasa A, Castiglioni I, Gallivanone F, Augimeri A, Lopez M, Arabia G, Morelli M, Gilardi MC, Quattrone A. Machine learning on brain MRI data for differential diagnosis of Parkinson’s disease and progressive supranuclear palsy. J Neurosci Methods. 2014;222:230–7.PubMed Salvatore C, Cerasa A, Castiglioni I, Gallivanone F, Augimeri A, Lopez M, Arabia G, Morelli M, Gilardi MC, Quattrone A. Machine learning on brain MRI data for differential diagnosis of Parkinson’s disease and progressive supranuclear palsy. J Neurosci Methods. 2014;222:230–7.PubMed
46.
go back to reference Cherubini A, Morelli M, Nisticó R, Salsone M, Arabia G, Vasta R, Augimeri A, Caligiuri ME, Quattrone A. Magnetic resonance support vector machine discriminates between Parkinson disease and progressive supranuclear palsy. Mov Disord. 2014;29:266–9.PubMed Cherubini A, Morelli M, Nisticó R, Salsone M, Arabia G, Vasta R, Augimeri A, Caligiuri ME, Quattrone A. Magnetic resonance support vector machine discriminates between Parkinson disease and progressive supranuclear palsy. Mov Disord. 2014;29:266–9.PubMed
47.
go back to reference Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, Obeso J, Marek K, Litvan I, Lang AE, Halliday G, Goetz CG, Gasser T, Dubois B, Chan P, Bloem BR, Adler CH, Deuschl G. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015;30:1591–601.PubMed Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, Obeso J, Marek K, Litvan I, Lang AE, Halliday G, Goetz CG, Gasser T, Dubois B, Chan P, Bloem BR, Adler CH, Deuschl G. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015;30:1591–601.PubMed
48.
go back to reference Boxer AL, Yu JT, Golbe LI, Litvan I, Lang AE, Höglinger GU. Advances in progressive supranuclear palsy: new diagnostic criteria, biomarkers, and therapeutic approaches. Lancet Neurol. 2017;16:552–63.PubMedPubMedCentral Boxer AL, Yu JT, Golbe LI, Litvan I, Lang AE, Höglinger GU. Advances in progressive supranuclear palsy: new diagnostic criteria, biomarkers, and therapeutic approaches. Lancet Neurol. 2017;16:552–63.PubMedPubMedCentral
Metadata
Title
Improved Automatic Morphology-Based Classification of Parkinson’s Disease and Progressive Supranuclear Palsy
Authors
Aron S. Talai
Zahinoor Ismail
Jan Sedlacik
Kai Boelmans
Nils D. Forkert
Publication date
01-12-2019
Publisher
Springer Berlin Heidelberg
Published in
Clinical Neuroradiology / Issue 4/2019
Print ISSN: 1869-1439
Electronic ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-018-0727-8

Other articles of this Issue 4/2019

Clinical Neuroradiology 4/2019 Go to the issue