Diagnosis of Early-Stage Idiopathic Parkinson's Disease Using High-Resolution Quantitative Susceptibility Mapping Combined with Histogram Analysis in the Substantia Nigra at 3 T

Background and Purpose To test whether nigrosome-1 imaging using high-resolution quantitative susceptibility mapping (QSM) combined with histogram analysis can improve the diagnostic accuracy in early-stage idiopathic Parkinson's disease (IPD) patients. Methods Three-dimensional multiecho gradient-recalled echo images (0.5×0.5×1.0 mm3) were obtained at 3 T for QSM in 38 patients with IPD and 25 healthy subjects. To segment the substantia nigra (SN), regions of interest (ROIs) were semiautomatically drawn at the location below the red nucleus, and the normal-appearing nigrosome-1 was determined by manual correction. QSM histograms were obtained within the ROI. The segmented SN regions on the right and left that had higher mean susceptibility values and fewer voxels with susceptibility values lower than 60, 65, 70, 75, and 80 ppb were chosen for comparisons between the IPD patients and healthy subjects. These results were compared with those of the visual assessments of nigrosome-1 in susceptibility map-weighted imaging (SMWI) by analyzing receiver operating characteristics curves. Results The proportion of voxels with susceptibility values lower than 70 ppb showed the best diagnostic performance, with its value differing significantly between the IPD patients (median=0, interquartile range=0–0.23) and healthy subjects (median=10.67, interquartile range=5.98–21.57) (p<0.0001). The number of voxels with susceptibility values lower than 60, 65, 70, 75, and 80 ppb showed worse diagnostic performances but were still significantly better than that of the mean susceptibility value (p=0.0249, 0.0192, 0.0183, 0.0191, and 0.0186, respectively), which also differed significantly between the two groups: 125.81±16.27 ppb (mean±standard deviation) in IPD versus 98.41±11.70 ppb in healthy subjects (p<0.0001). Additionally, using the proportion of voxels with susceptibility values lower than 70 ppb provided significantly better diagnostic performance than did visual assessments of SMWI (p=0.0143). Conclusions High-spatial-resolution QSM combined with histogram analysis at 3 T can improve the diagnostic accuracy of early-stage IPD.

[1]  Xuemei Huang,et al.  Quantitative susceptibility mapping of the midbrain in Parkinson's disease , 2016, Movement disorders : official journal of the Movement Disorder Society.

[2]  Tony F. Chan,et al.  Active contours without edges , 2001, IEEE Trans. Image Process..

[3]  Wei Cao,et al.  A method for estimating and removing streaking artifacts in quantitative susceptibility mapping , 2015, NeuroImage.

[4]  E. DeLong,et al.  Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. , 1988, Biometrics.

[5]  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.

[6]  Matthew J. Betts,et al.  The whole-brain pattern of magnetic susceptibility perturbations in Parkinson’s disease , 2017, Brain : a journal of neurology.

[7]  R. Bowtell,et al.  Visualization of nigrosome 1 and its loss in PD , 2013, Neurology.

[8]  Dong-Hyun Kim,et al.  Imaging of nigrosome 1 in substantia nigra at 3T using multiecho susceptibility map‐weighted imaging (SMWI) , 2017, Journal of magnetic resonance imaging : JMRI.

[9]  J. Lee,et al.  Nigrosome 1 Detection at 3T MRI for the Diagnosis of Early-Stage Idiopathic Parkinson Disease: Assessment of Diagnostic Accuracy and Agreement on Imaging Asymmetry and Clinical Laterality , 2015, American Journal of Neuroradiology.

[10]  Xue Xiao,et al.  Integrated Laplacian‐based phase unwrapping and background phase removal for quantitative susceptibility mapping , 2014, NMR in biomedicine.

[11]  Michael Schocke,et al.  Dorsolateral nigral hyperintensity on 3.0T susceptibility‐weighted imaging in neurodegenerative Parkinsonism , 2015, Movement disorders : official journal of the Movement Disorder Society.

[12]  Dorothee P. Auer,et al.  The ‘Swallow Tail’ Appearance of the Healthy Nigrosome – A New Accurate Test of Parkinson's Disease: A Case-Control and Retrospective Cross-Sectional MRI Study at 3T , 2014, PloS one.

[13]  Ji Young Yun,et al.  Loss of Nigral Hyperintensity on 3 Tesla MRI of Parkinsonism: Comparison With 123I‐FP‐CIT SPECT , 2016, Movement disorders : official journal of the Movement Disorder Society.

[14]  P-Y Lin,et al.  Quantitative Susceptibility Mapping of Human Brain at 3T: A Multisite Reproducibility Study , 2015, American Journal of Neuroradiology.

[15]  Pascal Spincemaille,et al.  Reproducibility of quantitative susceptibility mapping in the brain at two field strengths from two vendors , 2015, Journal of magnetic resonance imaging : JMRI.

[16]  E. Kim,et al.  Drug-induced Parkinsonism versus Idiopathic Parkinson Disease: Utility of Nigrosome 1 with 3-T Imaging. , 2016, Radiology.

[17]  Nian Wang,et al.  Regionally progressive accumulation of iron in Parkinson's disease as measured by quantitative susceptibility mapping , 2017, NMR in biomedicine.

[18]  M. Tosetti,et al.  Nigral involvement in atypical parkinsonisms: evidence from a pilot study with ultra-high field MRI , 2016, Journal of Neural Transmission.

[19]  E Mark Haacke,et al.  Quantifying brain iron deposition in patients with Parkinson's disease using quantitative susceptibility mapping, R2 and R2. , 2015, Magnetic resonance imaging.

[20]  N. Wang,et al.  Using ‘swallow-tail’ sign and putaminal hypointensity as biomarkers to distinguish multiple system atrophy from idiopathic Parkinson’s disease: A susceptibility-weighted imaging study , 2017, European Radiology.

[21]  Kemin Chen,et al.  Region‐specific disturbed iron distribution in early idiopathic Parkinson's disease measured by quantitative susceptibility mapping , 2015, Human brain mapping.

[22]  T. Simuni,et al.  Can loss of the swallow tail sign help distinguish between Parkinson Disease and the Parkinson-Plus syndromes? , 2017, Clinical imaging.

[23]  M. Tosetti,et al.  MR imaging of the substantia nigra at 7 T enables diagnosis of Parkinson disease. , 2014, Radiology.

[24]  Y Wang,et al.  Usefulness of Quantitative Susceptibility Mapping for the Diagnosis of Parkinson Disease , 2015, American Journal of Neuroradiology.

[25]  C Strand,et al.  9.4 T MR microscopy of the substantia nigra with pathological validation in controls and disease , 2016, NeuroImage: Clinical.

[26]  Ferdinand Schweser,et al.  Quantitative Susceptibility Mapping in Parkinson's Disease , 2016, PloS one.

[27]  Y Wang,et al.  Lateral Asymmetry and Spatial Difference of Iron Deposition in the Substantia Nigra of Patients with Parkinson Disease Measured with Quantitative Susceptibility Mapping , 2016, American Journal of Neuroradiology.

[28]  A. Graybiel,et al.  The substantia nigra of the human brain. I. Nigrosomes and the nigral matrix, a compartmental organization based on calbindin D(28K) immunohistochemistry. , 1999, Brain : a journal of neurology.

[29]  M. Fukunaga,et al.  Sensitivity of MRI resonance frequency to the orientation of brain tissue microstructure , 2010, Proceedings of the National Academy of Sciences.

[30]  M. Hoehn,et al.  Parkinsonism , 1967, Neurology.

[31]  M. Tosetti,et al.  Comparison of 3T and 7T Susceptibility-Weighted Angiography of the Substantia Nigra in Diagnosing Parkinson Disease , 2015, American Journal of Neuroradiology.