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Research ArticleAdult Brain
Open Access

Comparative Study of MRI Biomarkers in the Substantia Nigra to Discriminate Idiopathic Parkinson Disease

N. Pyatigorskaya, B. Magnin, M. Mongin, L. Yahia-Cherif, R. Valabregue, D. Arnaldi, C. Ewenczyk, C. Poupon, M. Vidailhet and S. Lehéricy
American Journal of Neuroradiology August 2018, 39 (8) 1460-1467; DOI: https://doi.org/10.3174/ajnr.A5702
N. Pyatigorskaya
aFrom the Institut du Cerveau et de la Moelle épinière (N.P., B.M., M.M., L.Y.-C., R.V., D.A., M.V., S.L.), Centre de NeuroImagerie de Recherche, Paris, France
bUMR S 1127, CNRS UMR 7225 (N.P., B.M., M.M., L.Y.-C., M.V., S.L.), Sorbonne University, Paris, France
cService de neuroradiologie (N.P., B.M., S.L.)
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B. Magnin
aFrom the Institut du Cerveau et de la Moelle épinière (N.P., B.M., M.M., L.Y.-C., R.V., D.A., M.V., S.L.), Centre de NeuroImagerie de Recherche, Paris, France
bUMR S 1127, CNRS UMR 7225 (N.P., B.M., M.M., L.Y.-C., M.V., S.L.), Sorbonne University, Paris, France
cService de neuroradiologie (N.P., B.M., S.L.)
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M. Mongin
aFrom the Institut du Cerveau et de la Moelle épinière (N.P., B.M., M.M., L.Y.-C., R.V., D.A., M.V., S.L.), Centre de NeuroImagerie de Recherche, Paris, France
bUMR S 1127, CNRS UMR 7225 (N.P., B.M., M.M., L.Y.-C., M.V., S.L.), Sorbonne University, Paris, France
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L. Yahia-Cherif
aFrom the Institut du Cerveau et de la Moelle épinière (N.P., B.M., M.M., L.Y.-C., R.V., D.A., M.V., S.L.), Centre de NeuroImagerie de Recherche, Paris, France
bUMR S 1127, CNRS UMR 7225 (N.P., B.M., M.M., L.Y.-C., M.V., S.L.), Sorbonne University, Paris, France
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R. Valabregue
aFrom the Institut du Cerveau et de la Moelle épinière (N.P., B.M., M.M., L.Y.-C., R.V., D.A., M.V., S.L.), Centre de NeuroImagerie de Recherche, Paris, France
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D. Arnaldi
aFrom the Institut du Cerveau et de la Moelle épinière (N.P., B.M., M.M., L.Y.-C., R.V., D.A., M.V., S.L.), Centre de NeuroImagerie de Recherche, Paris, France
eClinical Neurology (D.A.), Department of Neuroscience, University of Genoa, Genoa, Italy
gCentre d'Investigation Clinique (D.A., M.V.), Hôpital Pitié-Salpêtrière, Paris, France.
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C. Ewenczyk
dDépartement des Maladies du Système Nerveux (C.E., M.V.), Clinique des mouvements anormaux, Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Paris, France
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C. Poupon
fNeuroSpin (C.P.), Commissariat à l'Energie Atomique, Gif-Sur-Yvette, France
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M. Vidailhet
aFrom the Institut du Cerveau et de la Moelle épinière (N.P., B.M., M.M., L.Y.-C., R.V., D.A., M.V., S.L.), Centre de NeuroImagerie de Recherche, Paris, France
bUMR S 1127, CNRS UMR 7225 (N.P., B.M., M.M., L.Y.-C., M.V., S.L.), Sorbonne University, Paris, France
dDépartement des Maladies du Système Nerveux (C.E., M.V.), Clinique des mouvements anormaux, Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière, Paris, France
gCentre d'Investigation Clinique (D.A., M.V.), Hôpital Pitié-Salpêtrière, Paris, France.
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S. Lehéricy
aFrom the Institut du Cerveau et de la Moelle épinière (N.P., B.M., M.M., L.Y.-C., R.V., D.A., M.V., S.L.), Centre de NeuroImagerie de Recherche, Paris, France
bUMR S 1127, CNRS UMR 7225 (N.P., B.M., M.M., L.Y.-C., M.V., S.L.), Sorbonne University, Paris, France
cService de neuroradiologie (N.P., B.M., S.L.)
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    Fig 1.

    Segmentation of ROIs. Axial brain stem slices in a healthy volunteer (A) and a patient with Parkinson disease (B) show reduction of the neuromelanin signal intensity in the substantia nigra of the patient. Axial T2*WI 7T slices show dorsal nigral hyperintensity in a HV (C), which is absent in the patient with PD (D). T2WI axial (E) and coronal (F) images of the SN in a HV show T2-based segmentation of the SN.

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    Fig 2.

    Boxplot of the 3T NM SN volume (cubic millimeters) (A) and signal intensity ratio (B) (calculated by normalizing the mean signal of the SN in each slice to the signal in the background region), the 3T NM FA (C), and the 7T T2*WI SN volume (D) shows a reduction in all measures in patients with PD compared with HVs.

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    Fig 3.

    Receiver operating characteristic curves of the 3T NM volume, the 3T NM signal intensity ratio, the 3T NM FA, the 7T T2* volume (A), and the combination of the first 3 biomarkers for differentiating patients with PD from HVs (B).

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    Table 1:

    Quantitative measurements in the SNa

    SidePDHV
    3T NM ROI
        Volume
            L184.41 ± 68.84261.45 ± 47.68b
            R176.91 ± 62.89258.89 ± 46.62b
            Mean LR180.66 ± 63.63260.17 ± 42.87b
        Signal
            L106.74 ± 2.64110.21 ± 2.55b
            R106.61 ± 3.32110.46 ± 2.82b
            Mean LR110.56 ± 2.62110.33 ± 2.40b
        FA
            L0.32 ± 0.040.34 ± 0.04c
            R0.31 ± 0.040.33 ± 0.04
            Mean LR0.31 ± 0.030.33 ± 0.04c
        AD
            L0.68 ± 0.090.59 ± 0.10d
            R0.70 ± 0.080.62 ± 0.10c
            Mean LR0.69 ± 0.080.60 ± 0.10c
        RD
            L0.44 ± 0.060.38 ± 0.07d
            R0.46 ± 0.060.40 ± 0.07c
            Mean LR0.45 ± 0.060.39 ± 0.07c
        MD
            L0.52 ± 0.070.45 ± 0.08d
            R0.54 ± 0.060.48 ± 0.08c
            Mean LR0.53 ± 0.110.46 ± 0.08c
        R2*
            L35.91 ± 4.9536.66 ± 2.84
            R36.10 ± 6.6436.54 ± 2.80
            Mean LR35.65 ± 6.4636.60 ± 2.64
    3T T2 ROI
        FA
            L0.39 ± 0.060.42 ± 0.06
            R0.37 ± 0.060.40 ± 0.05
            Mean LR0.38 ± 0.060.40 ± 0.05
        AD
            L0.50 ± 0.090.45 ± 0.10
            R0.53 ± 0.100.49 ± 0.11
            Mean LR0.52 ± 0.090.47 ± 0.10
        RD
            L0.30 ± 0.060.26 ± 0.10c
            R0.33 ± 0.060.29 ± 0.06c
            Mean LR0.32 ± 0.060.28 ± 0.0c
        MD
            L0.37 ± 0.070.32 ± 0.07c
            R0.40 ± 0.070.35 ± 0.08c
            Mean LR0.38 ± 0.070.34 ± 0.08c
        R2*
            L28.47 ± 4.1730.21 ± 3.23
            R28.91 ± 3.9829.93 ± 2.87
            Mean LR28.69 ± 3.9730.07 ± 2.88
    7T T2*WI ROI
        T2WI volume
            L459.75 ± 120.74541.14 ± 118.80c
            R468.11 ± 130.00523.01 ± 121.85c
            Mean LR463.93 ± 122.83532.07 ± 118.33c
    • Note:—L indicates left; R, right; LR, average of left and right.

    • ↵a Quantitative measurements in the substantia nigra (mean and SD) are presented.

    • ↵b Significant differences between patients with PD and HVs are indicated using P < .001.

    • ↵c Significant differences between patients with PD and HVs are indicated using P < .05.

    • ↵d Significant differences between patients with PD and HVs are indicated using P < .005.

    • View popup
    Table 2:

    Diagnostic accuracy of quantitative and qualitative (visual) assessments

    SensitivitySpecificityPPVNPVAUC (95% CI)Diagnostic AccuracyCutoff
    Quantitative measurements
        3T NM signal0.880.80.880.80.88 (0.79–0.97)0.86110.35
        Volume10.720.8610.86 (0.76–0.95)0.89200.02
        7T T2*WI volume0.650.720.820.540.69 (0.53–0.84)0.68498.70
    Diffusion measures
        FA 3T NM0.750.530.750.550.68 (0.54–0.82)0.680.33
        3T T2WI0.650.700.80.520.64 (0.5–0.79)0.660.37
        AD 3T NM0.70.650.780.540.73 (0.59–0.87)0.680.64
        3T T2WI0.610.750.810.520.65 (0.49–0.80)0.660.5
        RD 3T NM0.640.750.820.540.72 (0.58–0.86)0.670.43
        3T T2WI0.720.60.760.550.68 (0.52–0.83)0.670.29
        MD 3T NM0.670.750.830.560.72 (0.58–0.87)0.70.51
        3T T2WI0.640.750.820.540.67 (0.53–0.82)0.670.38
    Combined measurements
        NM signal and volume + FA (3T NM)0.920.950.970.860.96 (0.9–1)0.934.4
    Qualitative evaluation
        NM at 3T0.830.90.940.9–0.86–
        DNH at 7T
            Method 10.970.80.90.94–0.91–
            Method 20.940.850.920.9–0.91–
    • Note:—AUC indicates area under the curve; NPV, negative predictive value; PPV, positive predictive value.

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N. Pyatigorskaya, B. Magnin, M. Mongin, L. Yahia-Cherif, R. Valabregue, D. Arnaldi, C. Ewenczyk, C. Poupon, M. Vidailhet, S. Lehéricy
Comparative Study of MRI Biomarkers in the Substantia Nigra to Discriminate Idiopathic Parkinson Disease
American Journal of Neuroradiology Aug 2018, 39 (8) 1460-1467; DOI: 10.3174/ajnr.A5702

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Comparative Study of MRI Biomarkers in the Substantia Nigra to Discriminate Idiopathic Parkinson Disease
N. Pyatigorskaya, B. Magnin, M. Mongin, L. Yahia-Cherif, R. Valabregue, D. Arnaldi, C. Ewenczyk, C. Poupon, M. Vidailhet, S. Lehéricy
American Journal of Neuroradiology Aug 2018, 39 (8) 1460-1467; DOI: 10.3174/ajnr.A5702
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