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Erschienen in: European Radiology 8/2018

12.03.2018 | Neuro

Extraction of large-scale structural covariance networks from grey matter volume for Parkinson’s disease classification

verfasst von: Pei-Lin Lee, Kun-Hsien Chou, Cheng-Hsien Lu, Hsiu-Ling Chen, Nai-Wen Tsai, Ai-Ling Hsu, Meng-Hsiang Chen, Wei-Che Lin, Ching-Po Lin

Erschienen in: European Radiology | Ausgabe 8/2018

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Abstract

Objectives

To identify disease-related spatial covariance patterns of grey matter volume as an aid in the classification of Parkinson’s disease (PD).

Methods

Seventy structural covariance networks (SCNs) based on grey matter volume covariance patterns were defined using independent component analysis with T1-weighted structural MRI scans (discovery sample, 70 PD patients and 70 healthy controls). An image-based classifier was constructed from SCNs using a multiple logistic regression analysis with a leave-one-out cross-validation-based feature selection scheme. A validation sample (26 PD patients and 26 healthy controls) was further collected to evaluate the generalization ability of the constructed classifier.

Results

In the discovery sample, 13 SCNs, including the cerebellum, anterior temporal poles, parahippocampal gyrus, parietal operculum, occipital lobes, supramarginal gyri, superior parietal lobes, paracingulate gyri and precentral gyri, had higher classification performance for PD. In the validation sample, the classifier had moderate generalization ability, with a mean sensitivity of 81%, specificity of 69% and overall accuracy of 75%. Furthermore, certain individual SCNs were also associated with disease severity.

Conclusions

Although not applicable for routine care at present, our results provide empirical evidence that disease-specific, large-scale structural networks can provide a foundation for the further improvement of diagnostic MRI in movement disorders.

Key Points

• Disease-specific, large-scale SCNs can be identified from structural MRI.
• A new network-based framework for PD classification is proposed.
• An SCN-based classifier had moderate generalization ability in PD classification.
• The selected SCNs provide valuable functional information regarding PD patients.
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Literatur
1.
Zurück zum Zitat Sveinbjornsdottir S (2016) The clinical symptoms of Parkinson's disease. J Neurochem 139:318–324CrossRefPubMed Sveinbjornsdottir S (2016) The clinical symptoms of Parkinson's disease. J Neurochem 139:318–324CrossRefPubMed
2.
Zurück zum Zitat Chaudhuri KR, Healy DG, Schapira AH, National Institute for Clinical Excellence (2006) Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurol 5:235–245CrossRefPubMed Chaudhuri KR, Healy DG, Schapira AH, National Institute for Clinical Excellence (2006) Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurol 5:235–245CrossRefPubMed
3.
Zurück zum Zitat Luo C, Song W, Chen Q et al (2014) Reduced functional connectivity in early-stage drug-naive Parkinson's disease: a resting-state fMRI study. Neurobiol Aging 35:431–441CrossRefPubMed Luo C, Song W, Chen Q et al (2014) Reduced functional connectivity in early-stage drug-naive Parkinson's disease: a resting-state fMRI study. Neurobiol Aging 35:431–441CrossRefPubMed
4.
Zurück zum Zitat Pan PL, Song W, Shang HF (2012) Voxel-wise meta-analysis of gray matter abnormalities in idiopathic Parkinson's disease. Eur J Neurol 19:199–206CrossRefPubMed Pan PL, Song W, Shang HF (2012) Voxel-wise meta-analysis of gray matter abnormalities in idiopathic Parkinson's disease. Eur J Neurol 19:199–206CrossRefPubMed
5.
Zurück zum Zitat Tessitore A, Amboni M, Cirillo G et al (2012) Regional gray matter atrophy in patients with Parkinson disease and freezing of gait. AJNR Am J Neuroradiol 33:1804–1809CrossRefPubMed Tessitore A, Amboni M, Cirillo G et al (2012) Regional gray matter atrophy in patients with Parkinson disease and freezing of gait. AJNR Am J Neuroradiol 33:1804–1809CrossRefPubMed
6.
Zurück zum Zitat Tessitore A, Santangelo G, De Micco R et al (2016) Cortical thickness changes in patients with Parkinson's disease and impulse control disorders. Parkinsonism Relat Disord 24:119–125CrossRefPubMed Tessitore A, Santangelo G, De Micco R et al (2016) Cortical thickness changes in patients with Parkinson's disease and impulse control disorders. Parkinsonism Relat Disord 24:119–125CrossRefPubMed
7.
Zurück zum Zitat Mak E, Su L, Williams GB et al (2015) Baseline and longitudinal grey matter changes in newly diagnosed Parkinson's disease: ICICLE-PD study. Brain 138:2974–2986CrossRefPubMedPubMedCentral Mak E, Su L, Williams GB et al (2015) Baseline and longitudinal grey matter changes in newly diagnosed Parkinson's disease: ICICLE-PD study. Brain 138:2974–2986CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Mechelli A, Friston KJ, Frackowiak RS, Price CJ (2005) Structural covariance in the human cortex. J Neurosci 25:8303–8310CrossRefPubMed Mechelli A, Friston KJ, Frackowiak RS, Price CJ (2005) Structural covariance in the human cortex. J Neurosci 25:8303–8310CrossRefPubMed
9.
Zurück zum Zitat Chou KH, Lin WC, Lee PL et al (2015) Structural covariance networks of striatum subdivision in patients with Parkinson's disease. Hum Brain Mapp 36:1567–1584CrossRefPubMed Chou KH, Lin WC, Lee PL et al (2015) Structural covariance networks of striatum subdivision in patients with Parkinson's disease. Hum Brain Mapp 36:1567–1584CrossRefPubMed
10.
11.
Zurück zum Zitat Pagani M, Bifone A, Gozzi A (2016) Structural covariance networks in the mouse brain. NeuroImage 129:55–63CrossRefPubMed Pagani M, Bifone A, Gozzi A (2016) Structural covariance networks in the mouse brain. NeuroImage 129:55–63CrossRefPubMed
12.
Zurück zum Zitat Paviour DC, Price SL, Stevens JM, Lees AJ, Fox NC (2005) Quantitative MRI measurement of superior cerebellar peduncle in progressive supranuclear palsy. Neurology 64:675–679CrossRefPubMed Paviour DC, Price SL, Stevens JM, Lees AJ, Fox NC (2005) Quantitative MRI measurement of superior cerebellar peduncle in progressive supranuclear palsy. Neurology 64:675–679CrossRefPubMed
13.
Zurück zum Zitat Marquand AF, Filippone M, Ashburner J et al (2013) Automated, high accuracy classification of Parkinsonian disorders: a pattern recognition approach. PLoS One 8:e69237CrossRefPubMedPubMedCentral Marquand AF, Filippone M, Ashburner J et al (2013) Automated, high accuracy classification of Parkinsonian disorders: a pattern recognition approach. PLoS One 8:e69237CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Lin WC, Chou KH, Lee PL et al (2017) Parkinson's disease: diagnostic utility of volumetric imaging. Neuroradiology 59:367–377CrossRefPubMed Lin WC, Chou KH, Lee PL et al (2017) Parkinson's disease: diagnostic utility of volumetric imaging. Neuroradiology 59:367–377CrossRefPubMed
15.
Zurück zum Zitat Fornito A, Zalesky A, Breakspear M (2015) The connectomics of brain disorders. Nat Rev Neurosci 16:159–172CrossRefPubMed Fornito A, Zalesky A, Breakspear M (2015) The connectomics of brain disorders. Nat Rev Neurosci 16:159–172CrossRefPubMed
16.
Zurück zum Zitat Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD (2009) Neurodegenerative diseases target large-scale human brain networks. Neuron 62:42–52CrossRefPubMedPubMedCentral Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD (2009) Neurodegenerative diseases target large-scale human brain networks. Neuron 62:42–52CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Willette AA, Calhoun VD, Egan JM, Kapogiannis D, Alzheimers Disease Neuroimaging Initiative (2014) Prognostic classification of mild cognitive impairment and Alzheimer's disease: MRI independent component analysis. Psychiatry Res 224:81–88CrossRefPubMedPubMedCentral Willette AA, Calhoun VD, Egan JM, Kapogiannis D, Alzheimers Disease Neuroimaging Initiative (2014) Prognostic classification of mild cognitive impairment and Alzheimer's disease: MRI independent component analysis. Psychiatry Res 224:81–88CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Hafkemeijer A, Moller C, Dopper EG et al (2016) Differences in structural covariance brain networks between behavioral variant frontotemporal dementia and Alzheimer's disease. Hum Brain Mapp 37:978–988CrossRefPubMed Hafkemeijer A, Moller C, Dopper EG et al (2016) Differences in structural covariance brain networks between behavioral variant frontotemporal dementia and Alzheimer's disease. Hum Brain Mapp 37:978–988CrossRefPubMed
20.
Zurück zum Zitat Rektorova I, Biundo R, Marecek R, Weis L, Aarsland D, Antonini A (2014) Grey matter changes in cognitively impaired Parkinson's disease patients. PLoS One 9:e85595CrossRefPubMedPubMedCentral Rektorova I, Biundo R, Marecek R, Weis L, Aarsland D, Antonini A (2014) Grey matter changes in cognitively impaired Parkinson's disease patients. PLoS One 9:e85595CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Postuma RB, Berg D, Stern M et al (2015) MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord 30:1591–1601CrossRefPubMed Postuma RB, Berg D, Stern M et al (2015) MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord 30:1591–1601CrossRefPubMed
23.
Zurück zum Zitat Gasser T, Bressman S, Durr A, Higgins J, Klockgether T, Myers RH (2003) State of the art review: molecular diagnosis of inherited movement disorders. Movement Disorders Society task force on molecular diagnosis. Mov Disord 18:3–18CrossRefPubMed Gasser T, Bressman S, Durr A, Higgins J, Klockgether T, Myers RH (2003) State of the art review: molecular diagnosis of inherited movement disorders. Movement Disorders Society task force on molecular diagnosis. Mov Disord 18:3–18CrossRefPubMed
24.
Zurück zum Zitat Goetz CG, Poewe W, Rascol O et al (2004) Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations. Mov Disord 19:1020–1028CrossRefPubMed Goetz CG, Poewe W, Rascol O et al (2004) Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations. Mov Disord 19:1020–1028CrossRefPubMed
25.
Zurück zum Zitat Schwab RS, Engeland A (1969) Projection technique for evaluating surgery in Parkinson's disease. Livingstone, Edinburgh Schwab RS, Engeland A (1969) Projection technique for evaluating surgery in Parkinson's disease. Livingstone, Edinburgh
26.
Zurück zum Zitat Ashburner J, Friston KJ (2000) Voxel-based morphometry–the methods. NeuroImage 11:805–821CrossRefPubMed Ashburner J, Friston KJ (2000) Voxel-based morphometry–the methods. NeuroImage 11:805–821CrossRefPubMed
27.
Zurück zum Zitat Yang FC, Chou KH, Fuh JL et al (2013) Altered gray matter volume in the frontal pain modulation network in patients with cluster headache. Pain 154:801–807CrossRefPubMed Yang FC, Chou KH, Fuh JL et al (2013) Altered gray matter volume in the frontal pain modulation network in patients with cluster headache. Pain 154:801–807CrossRefPubMed
28.
Zurück zum Zitat Douaud G, Groves AR, Tamnes CK et al (2014) A common brain network links development, aging, and vulnerability to disease. Proc Natl Acad Sci U S A 111:17648–17653CrossRefPubMedPubMedCentral Douaud G, Groves AR, Tamnes CK et al (2014) A common brain network links development, aging, and vulnerability to disease. Proc Natl Acad Sci U S A 111:17648–17653CrossRefPubMedPubMedCentral
29.
30.
Zurück zum Zitat Smith SM, Fox PT, Miller KL et al (2009) Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci U S A 106:13040–13045CrossRefPubMedPubMedCentral Smith SM, Fox PT, Miller KL et al (2009) Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci U S A 106:13040–13045CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Filippini N, MacIntosh BJ, Hough MG et al (2009) Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci U S A 106:7209–7214CrossRefPubMedPubMedCentral Filippini N, MacIntosh BJ, Hough MG et al (2009) Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci U S A 106:7209–7214CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Perkins NJ, Schisterman EF (2006) The inconsistency of "optimal" cutpoints obtained using two criteria based on the receiver operating characteristic curve. Am J Epidemiol 163:670–675CrossRefPubMedPubMedCentral Perkins NJ, Schisterman EF (2006) The inconsistency of "optimal" cutpoints obtained using two criteria based on the receiver operating characteristic curve. Am J Epidemiol 163:670–675CrossRefPubMedPubMedCentral
33.
Zurück zum Zitat van Stralen KJ, Stel VS, Reitsma JB, Dekker FW, Zoccali C, Jager KJ (2009) Diagnostic methods I: sensitivity, specificity, and other measures of accuracy. Kidney Int 75:1257–1263CrossRefPubMed van Stralen KJ, Stel VS, Reitsma JB, Dekker FW, Zoccali C, Jager KJ (2009) Diagnostic methods I: sensitivity, specificity, and other measures of accuracy. Kidney Int 75:1257–1263CrossRefPubMed
34.
Zurück zum Zitat Nagelkerke NJD (1991) A note on a general definition of the coefficient of determination. Biometrika 78:691–692CrossRef Nagelkerke NJD (1991) A note on a general definition of the coefficient of determination. Biometrika 78:691–692CrossRef
35.
Zurück zum Zitat Ortiz A, Munilla J, Alvarez-Illan I, Gorriz JM, Ramirez J, Alzheimer's Disease Neuroimaging Initiative (2015) Exploratory graphical models of functional and structural connectivity patterns for Alzheimer's Disease diagnosis. Front Comput Neurosci 9:132CrossRefPubMedPubMedCentral Ortiz A, Munilla J, Alvarez-Illan I, Gorriz JM, Ramirez J, Alzheimer's Disease Neuroimaging Initiative (2015) Exploratory graphical models of functional and structural connectivity patterns for Alzheimer's Disease diagnosis. Front Comput Neurosci 9:132CrossRefPubMedPubMedCentral
36.
Zurück zum Zitat Ng B, Varoquaux G, Poline JB, Thirion B, Greicius MD, Poston KL (2017) Distinct alterations in Parkinson's medication-state and disease-state connectivity. Neuroimage Clin 16:575–585CrossRefPubMedPubMedCentral Ng B, Varoquaux G, Poline JB, Thirion B, Greicius MD, Poston KL (2017) Distinct alterations in Parkinson's medication-state and disease-state connectivity. Neuroimage Clin 16:575–585CrossRefPubMedPubMedCentral
37.
Zurück zum Zitat Zhang D, Liu X, Chen J, Liu B (2014) Distinguishing patients with Parkinson's disease subtypes from normal controls based on functional network regional efficiencies. PLoS One 9:e115131CrossRefPubMedPubMedCentral Zhang D, Liu X, Chen J, Liu B (2014) Distinguishing patients with Parkinson's disease subtypes from normal controls based on functional network regional efficiencies. PLoS One 9:e115131CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat Wang JJ, Lin WY, Lu CS et al (2011) Parkinson disease: diagnostic utility of diffusion kurtosis imaging. Radiology 261:210–217CrossRefPubMed Wang JJ, Lin WY, Lu CS et al (2011) Parkinson disease: diagnostic utility of diffusion kurtosis imaging. Radiology 261:210–217CrossRefPubMed
39.
Zurück zum Zitat Mahlknecht P, Krismer F, Poewe W, Seppi K (2017) Meta-analysis of dorsolateral nigral hyperintensity on magnetic resonance imaging as a marker for Parkinson's disease. Mov Disord 32:619–623CrossRefPubMed Mahlknecht P, Krismer F, Poewe W, Seppi K (2017) Meta-analysis of dorsolateral nigral hyperintensity on magnetic resonance imaging as a marker for Parkinson's disease. Mov Disord 32:619–623CrossRefPubMed
40.
Zurück zum Zitat Szewczyk-Krolikowski K, Menke RA, Rolinski M et al (2014) Functional connectivity in the basal ganglia network differentiates PD patients from controls. Neurology 83:208–214CrossRefPubMedPubMedCentral Szewczyk-Krolikowski K, Menke RA, Rolinski M et al (2014) Functional connectivity in the basal ganglia network differentiates PD patients from controls. Neurology 83:208–214CrossRefPubMedPubMedCentral
41.
42.
Zurück zum Zitat Lenka A, Naduthota RM, Jha M et al (2016) Freezing of gait in Parkinson's disease is associated with altered functional brain connectivity. Parkinsonism Relat Disord 24:100–106CrossRefPubMed Lenka A, Naduthota RM, Jha M et al (2016) Freezing of gait in Parkinson's disease is associated with altered functional brain connectivity. Parkinsonism Relat Disord 24:100–106CrossRefPubMed
43.
Zurück zum Zitat Leh SE, Petrides M, Strafella AP (2010) The neural circuitry of executive functions in healthy subjects and Parkinson's disease. Neuropsychopharmacology 35:70–85CrossRefPubMed Leh SE, Petrides M, Strafella AP (2010) The neural circuitry of executive functions in healthy subjects and Parkinson's disease. Neuropsychopharmacology 35:70–85CrossRefPubMed
44.
Zurück zum Zitat Carlesimo GA, Piras F, Assogna F, Pontieri FE, Caltagirone C, Spalletta G (2012) Hippocampal abnormalities and memory deficits in Parkinson disease: a multimodal imaging study. Neurology 78:1939–1945CrossRefPubMed Carlesimo GA, Piras F, Assogna F, Pontieri FE, Caltagirone C, Spalletta G (2012) Hippocampal abnormalities and memory deficits in Parkinson disease: a multimodal imaging study. Neurology 78:1939–1945CrossRefPubMed
45.
Zurück zum Zitat Cardoso EF, Fregni F, Maia FM et al (2010) Abnormal visual activation in Parkinson's disease patients. Mov Disord 25:1590–1596CrossRefPubMed Cardoso EF, Fregni F, Maia FM et al (2010) Abnormal visual activation in Parkinson's disease patients. Mov Disord 25:1590–1596CrossRefPubMed
46.
Zurück zum Zitat Luppino G, Matelli M, Camarda R, Rizzolatti G (1993) Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol 338:114–140CrossRefPubMed Luppino G, Matelli M, Camarda R, Rizzolatti G (1993) Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol 338:114–140CrossRefPubMed
47.
Zurück zum Zitat Cerasa A, Pugliese P, Messina D et al (2012) Prefrontal alterations in Parkinson's disease with levodopa-induced dyskinesia during fMRI motor task. Mov Disord 27:364–371CrossRefPubMed Cerasa A, Pugliese P, Messina D et al (2012) Prefrontal alterations in Parkinson's disease with levodopa-induced dyskinesia during fMRI motor task. Mov Disord 27:364–371CrossRefPubMed
48.
Zurück zum Zitat Sawada M, Imamura K, Nagatsu T (2006) Role of cytokines in inflammatory process in Parkinson's disease. J Neural Transm Suppl: 373–381 Sawada M, Imamura K, Nagatsu T (2006) Role of cytokines in inflammatory process in Parkinson's disease. J Neural Transm Suppl: 373–381
49.
Zurück zum Zitat Monchi O, Petrides M, Mejia-Constain B, Strafella AP (2007) Cortical activity in Parkinson's disease during executive processing depends on striatal involvement. Brain 130:233–244CrossRefPubMed Monchi O, Petrides M, Mejia-Constain B, Strafella AP (2007) Cortical activity in Parkinson's disease during executive processing depends on striatal involvement. Brain 130:233–244CrossRefPubMed
Metadaten
Titel
Extraction of large-scale structural covariance networks from grey matter volume for Parkinson’s disease classification
verfasst von
Pei-Lin Lee
Kun-Hsien Chou
Cheng-Hsien Lu
Hsiu-Ling Chen
Nai-Wen Tsai
Ai-Ling Hsu
Meng-Hsiang Chen
Wei-Che Lin
Ching-Po Lin
Publikationsdatum
12.03.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 8/2018
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5342-1

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