Neurite orientation dispersion and density imaging in the substantia nigra in idiopathic Parkinson disease

AbstractObjectivesWe used neurite orientation dispersion and density imaging (NODDI) to quantify changes in the substantia nigra pars compacta (SNpc) and striatum in Parkinson disease (PD).MethodsDiffusion-weighted magnetic resonance images were acquired from 58 PD patients and 36 age- and sex-matched controls. The intracellular volume fraction (Vic), orientation dispersion index (OD), and isotropic volume fraction (Viso) of the basal ganglia were compared between groups. Multivariate logistic regression analysis determined which diffusion parameters were independent predictors of PD. Receiver operating characteristic (ROC) analysis compared the diagnostic accuracies of the evaluated indices. Pearson coefficient analysis correlated each diffusional parameter with disease severity.ResultsVic in the contralateral SNpc and putamen were significantly lower in PD patients than in healthy controls (P < 0.00058). Vic and OD in the SNpc and putamen showed significant negative correlations (P < 0.05) with disease severity. Multivariate logistic analysis revealed that Vic (P = 0.0000046) and mean diffusivity (P = 0.019) in the contralateral SNpc were the independent predictors of PD. In the ROC analysis, Vic in the contralateral SNpc showed the best diagnostic performance (mean cutoff, 0.62; sensitivity, 0.88; specificity, 0.83).ConclusionNODDI is likely to be useful for diagnosing PD and assessing its progression.Key Points• Neurite orientation dispersion and density imaging (NODDI) is a new diffusion MRI technique • NODDI estimates neurite microstructure more specifically than diffusion tensor imaging • By using NODDI, nigrostriatal alterations in PD can be evaluated in vivo • NOODI is useful for diagnosing PD and assessing its disease progression

[1]  Dorothee P. Auer,et al.  Diffusion tensor imaging of nigral degeneration in Parkinson's disease: A region-of-interest and voxel-based study at 3 T and systematic review with meta-analysis☆ , 2013, NeuroImage: Clinical.

[2]  J. Helpern,et al.  Diffusional kurtosis imaging: The quantification of non‐gaussian water diffusion by means of magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[3]  Nin Bajaj,et al.  Clinical utility of dopamine transporter single photon emission CT (DaT-SPECT) with (123I) ioflupane in diagnosis of parkinsonian syndromes , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[4]  Paul M. Matthews,et al.  Connectivity-based segmentation of the substantia nigra in human and its implications in Parkinson's disease , 2010, NeuroImage.

[5]  J. Seibyl,et al.  The molecular basis of dopaminergic brain imaging in Parkinson's disease. , 2012, The quarterly journal of nuclear medicine and molecular imaging : official publication of the Italian Association of Nuclear Medicine (AIMN) [and] the International Association of Radiopharmacology (IAR), [and] Section of the Society of....

[6]  P. Svenningsson,et al.  MRI diffusion in Parkinson's disease: using the technique's inherent directional information to study the olfactory bulb and substantia nigra. , 2012, Journal of Parkinson's disease.

[7]  Y Nakata,et al.  Early pathological changes in the parkinsonian brain demonstrated by diffusion tensor MRI , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[8]  P. Basser,et al.  Toward a quantitative assessment of diffusion anisotropy , 1996, Magnetic resonance in medicine.

[9]  D R Rajput,et al.  Accuracy of clinical diagnosis of idiopathic Parkinson's disease. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[10]  C. Scherfler,et al.  Diffusion tensor imaging and olfactory identification testing in early-stage Parkinson's disease , 2011, Journal of Neurology.

[11]  Martin Styner,et al.  Imaging nigral pathology and clinical progression in Parkinson's disease , 2012, Movement disorders : official journal of the Movement Disorder Society.

[12]  Wang Zhan,et al.  Regional alterations of brain microstructure in Parkinson's disease using diffusion tensor imaging , 2012, Movement disorders : official journal of the Movement Disorder Society.

[13]  Y. Sitoh,et al.  Asymmetrical diffusion tensor imaging indices of the rostral substantia nigra in Parkinson's disease. , 2012, Parkinsonism & related disorders.

[14]  Paul M. Matthews,et al.  MRI characteristics of the substantia nigra in Parkinson's disease: A combined quantitative T1 and DTI study , 2009, NeuroImage.

[15]  P. Boesiger,et al.  Reduced field‐of‐view MRI using outer volume suppression for spinal cord diffusion imaging , 2007, Magnetic resonance in medicine.

[16]  Patrice Péran,et al.  Voxel‐based analysis of R2* maps in the healthy human brain , 2007, Journal of magnetic resonance imaging : JMRI.

[17]  A. Lozano,et al.  THE DOPAMINERGIC NIGROSTRIATAL SYSTEMAND PARKINSON'S DISEASE: MOLECULAR EVENTSIN DEVELOPMENT, DISEASE, AND CELL DEATH, AND NEW THERAPEUTIC STRATEGIES , 2007, Neurosurgery.

[18]  A. Deutch,et al.  Striatal plasticity in parkinsonism: dystrophic changes in medium spiny neurons and progression in Parkinson's disease. , 2006, Journal of neural transmission. Supplementum.

[19]  H. Braak,et al.  Staging of brain pathology related to sporadic Parkinson’s disease , 2003, Neurobiology of Aging.

[20]  A. Albanese,et al.  White Matter Involvement in Idiopathic Parkinson Disease: A Diffusion Tensor Imaging Study , 2009, American Journal of Neuroradiology.

[21]  Guy B. Williams,et al.  Absolute diffusivities define the landscape of white matter degeneration in Alzheimer's disease. , 2010, Brain : a journal of neurology.

[22]  W. Oertel,et al.  Relationship between clinical features of Parkinson's disease and presynaptic dopamine transporter binding assessed with [123I]IPT and single-photon emission tomography , 1997, European Journal of Nuclear Medicine.

[23]  Daniel C. Alexander,et al.  NODDI: Practical in vivo neurite orientation dispersion and density imaging of the human brain , 2012, NeuroImage.

[24]  A. Leemans,et al.  Characterizing the microstructural basis of “unidentified bright objects” in neurofibromatosis type 1: A combined in vivo multicomponent T2 relaxation and multi-shell diffusion MRI analysis , 2014, NeuroImage: Clinical.

[25]  T. Montine,et al.  Dendritic degeneration in neostriatal medium spiny neurons in Parkinson disease , 2005, Neurology.

[26]  Yi-Hsin Weng,et al.  Parkinson disease: diagnostic utility of diffusion kurtosis imaging. , 2011, Radiology.

[27]  W. Schulz-Schaeffer The synaptic pathology of α-synuclein aggregation in dementia with Lewy bodies, Parkinson’s disease and Parkinson’s disease dementia , 2010, Acta Neuropathologica.

[28]  H. Gertz,et al.  Pathological changes in dendrites of substantia nigra neurons in Parkinson's disease: a Golgi study. , 1991, Histology and histopathology.

[29]  A. Stefani,et al.  Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. , 2010, Brain : a journal of neurology.

[30]  C Trenkwalder,et al.  Differentiation of Typical and Atypical Parkinson Syndromes by Quantitative MR Imaging , 2011, American Journal of Neuroradiology.

[31]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[32]  J. Hughes,et al.  Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[33]  Martin Styner,et al.  Combined R2* and Diffusion Tensor Imaging Changes in the Substantia Nigra in Parkinson's Disease , 2011, Movement disorders : official journal of the Movement Disorder Society.

[34]  S Fook-Chong,et al.  Case control study of diffusion tensor imaging in Parkinson’s disease , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

[35]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[36]  S. Glantz,et al.  Primer of Applied Regression & Analysis of Variance , 1990 .

[37]  Haruyasu Yamada,et al.  Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis , 2002, Neurobiology of Aging.

[38]  M. B. Spraker,et al.  High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease , 2009, Neurology.

[39]  Hui Zhang,et al.  Advanced diffusion imaging sequences could aid assessing patients with focal cortical dysplasia and epilepsy☆ , 2014, Epilepsy Research.

[40]  A. Lees,et al.  Ageing and Parkinson's disease: substantia nigra regional selectivity. , 1991, Brain : a journal of neurology.