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Research ArticleNEURODEGENERATIVE DISORDER IMAGING

Imaging Biomarker for Early-Stage Alzheimer Disease: Utility of Hippocampal Histogram Analysis of Diffusion Metrics

Hiroto Takahashi, Yoichi Takami, Shuko Takeda, Naoki Hayakawa, Tsuneo Nakajima, Yasushi Takeya, Chisato Matsuo-Hagiyama, Atsuko Arisawa, Hiromi Rakugi and Noriyuki Tomiyama
American Journal of Neuroradiology February 2024, DOI: https://doi.org/10.3174/ajnr.A8106
Hiroto Takahashi
aFrom the Department of Diagnostic and Interventional Radiology (H.T., C.M.-H., A.A., N.T.), Osaka University Graduate School of Medicine, Suita, Osaka, Japan
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  • ORCID record for Hiroto Takahashi
Yoichi Takami
bDepartment of Geriatric and General Medicine (Y. Takami, N.H., T.N., Y. Takeya, H.R.), Osaka University Graduate School of Medicine, Suita, Osaka, Japan
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Shuko Takeda
cDepartment of Clinical Gene Therapy, Graduate School of Medicine (S.T.), Osaka University, Suita, Osaka, Japan
dOsaka Psychiatric Research Center (S.T.), Osaka Psychiatric Medical Center, Hirakata, Osaka, Japan
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Naoki Hayakawa
bDepartment of Geriatric and General Medicine (Y. Takami, N.H., T.N., Y. Takeya, H.R.), Osaka University Graduate School of Medicine, Suita, Osaka, Japan
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Tsuneo Nakajima
bDepartment of Geriatric and General Medicine (Y. Takami, N.H., T.N., Y. Takeya, H.R.), Osaka University Graduate School of Medicine, Suita, Osaka, Japan
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Yasushi Takeya
bDepartment of Geriatric and General Medicine (Y. Takami, N.H., T.N., Y. Takeya, H.R.), Osaka University Graduate School of Medicine, Suita, Osaka, Japan
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Chisato Matsuo-Hagiyama
aFrom the Department of Diagnostic and Interventional Radiology (H.T., C.M.-H., A.A., N.T.), Osaka University Graduate School of Medicine, Suita, Osaka, Japan
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  • ORCID record for Chisato Matsuo-Hagiyama
Atsuko Arisawa
aFrom the Department of Diagnostic and Interventional Radiology (H.T., C.M.-H., A.A., N.T.), Osaka University Graduate School of Medicine, Suita, Osaka, Japan
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Hiromi Rakugi
bDepartment of Geriatric and General Medicine (Y. Takami, N.H., T.N., Y. Takeya, H.R.), Osaka University Graduate School of Medicine, Suita, Osaka, Japan
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Noriyuki Tomiyama
aFrom the Department of Diagnostic and Interventional Radiology (H.T., C.M.-H., A.A., N.T.), Osaka University Graduate School of Medicine, Suita, Osaka, Japan
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Article Figures & Data

Figures

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  • FIG 1.
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    FIG 1.

    Inclusion and exclusion criteria.

  • FIG 2.
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    FIG 2.

    A b0 image showing the 3-section axial ROI that was created manually for each side of the hippocampus.

  • FIG 3.
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    FIG 3.

    Receiver operating characteristic curve of each logistic regression model for each diffusion parameter and volumetry. The diffusion parameter values are from the ROIs of each of observer A and observer B.

  • FIG 4.
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    FIG 4.

    R absolute value (|R|) of the left hippocampal values in the AzD group. Heat map of the correlations between the diffusion metrics and the volume. Values of 0.34 < |R| < 0.43 indicate a statistically significant difference with P < .05. Values of 0.43 < |R| indicate a statistically significant difference with P < .01.

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    Table 1:

    Detailed demographic and clinical data of patients with MCI

    Groupnon-AzDAzD
    Number3435
    Age (Median ± SD)78 ± 9.1579 ± 6.58
    Sex (M:F)18:1617:18
    MMSE (Median ± SD)26 ± 5.0924 ± 3.81
    ADAS-Cog (Median ± SD)9.40 ± 6.91a11.60 ± 4.19a
    RBMT (Median ± SD)11 ± 6.38a6.5 ± 4.99a
    P-tau/Aβ42 ratio0.05 ± 0.010.18 ± 0.07
    Aβ42 (pg/mL)919.38 ± 323.78a554.94 ± 148.24a
    P-tau (pg/mL)46.47 ± 15.36a91.37 ± 28.69a
    • Note:—MMSE indicates Mini-Mental State Examination; ADAS-Cog, Assessment Scale–Cognitive Subscale; RBMT, Rivermead Behavioral Memory Test; Aβ42, β-amyloid 42; P-tau, phosphorylated tau.

    • ↵a Statistically significant difference between the groups (P < .05).

    • View popup
    Table 2:

    ICCsa of the left and right hippocampal ROI values

    LeftRight
    NODDIICCICC
     ICVF (mean)0.87 (0.65−0.94)0.91 (0.86−0.94)
     Viso (mean)0.07 (−0.06−0.23)0.12 (−0.07−0.31)
    ODI (mean)0.70 (0.36−0.85)0.74 (0.52−0.85)
    DTI
     FA (mean)0.68 (0.53−0.79)0.59 (0.41−0.72)
     MD (mean)0.86 (0.40−0.95)0.84 (0.69−0.91)
     AD (mean)0.82 (0.31−0.93)0.84 (0.39−0.94)
     RD (mean)0.77 (0.53−0.88)0.84 (0.65−0.92)
    • Note:—ICCs indicates intraclass correlation coefficient.

    • ↵a The data in parentheses are 95% confidence intervals.

    • View popup
    Table 3:

    Statistically significant intergroup differences (P < .05) in the left and right hippocampal ROI values

    Hippocampal ROI (Observer A)Hippocampal ROI (Observer B)
    Value (Mean ± Standard Deviation)P ValueValue (Mean ± Standard Deviation)P Value
    non-AzDAzDnon-AzDAzD
    NODDI parameter
    Left ICVF (dimensionless)
     Mean0.377 ± 0.0320.358 ± 0.031.0080.366 ± 0.0330.349 ± 0.033.026
     90th percentile0.474 ± 0.0410.452 ± 0.047.0320.469 ± 0.0930.438 ± 0.049.029
    DTI parameter
    Right MD (mm2/s)
     Mean0.699 ± 0.0300.715 ± 0.031.0220.707 ± 0.0310.723 ± 0.030.046
    Left MD (mm2/s)
     Mean0.706 ± 0.0330.726 ± 0.034.0040.721 ± 0.0380.739 ± 0.039.014
     10th percentile0.641 ± 0.0320.666 ± 0.032.0010.658 ± 0.0350.676 ± 0.039.011
     90th percentile0.769 ± 0.0420.787 ± 0.040.0290.787 ± 0.0580.803 ± 0.047.026
    Left AD (mm2/s)
     Mean0.790 ± 0.0350.812 ± 0.036.0020.809 ± 0.0430.829 ± 0.039.008
     10th percentile0.716 ± 0.0330.739 ± 0.036.0010.733 ± 0.0380.753 ± 0.040.003
     90th percentile0.869 ± 0.0450.887 ± 0.042.0370.894 ± 0.0690.912 ± 0.051.039
    Left RD (mm2/s)
     Minimum0.531 ± 0.0530.556 ± 0.053.0280.543 ± 0.0760.564 ± 0.066.044
     Mean0.663 ± 0.0330.682 ± 0.034.0060.676 ± 0.0360.697 ± 0.047.013
     90th percentile0.730 ± 0.0400.747 ± 0.038.0380.745 ± 0.0540.771 ± 0.076.027
    Volume (mm3)
     Left3148.913 ± 519.8842872.464 ± 488.542.006
     Right3236.159 ± 438.5473015.669 ± 423.202.017
    • View popup
    Table 4:

    The logistic regression model used in the prediction of the intergroup differences

    AUCaOdds Ratio
    Logit (p)Diffusion ParameterVolumeAge/SexMMSE/ADAs-Cog/RBMTIntercept Term
    NODDI parameter
    Left ICVF (mean)
     Observer A0.69 (0.56−0.82)0.001.000.91/1.711.19/1.00/0.8120682.03
     Observer B0.68 (0.55−0.81)0.001.000.91/1.791.19/1.02/0.823487.07
    DTI parameter
    Right MD (mean)
     Observer A0.69 (0.56−0.82)159.681.000.91/1.731.19/1.01/0.8235.23
     Observer B0.68 (0.55−0.81)31.011.000.91/1.691.17/1.00/0.82238.04
    Left MD (10th percentile)
     Observer A0.73 (0.61−0.85)199854741945.311.000.91/2.081.22/1.02/0.790.00
     Observer B0.68 (0.55−0.81)126.301.000.91/1.911.19/1.02/0.828.02
    Left AD (10th percentile)
     Observer A0.71 (0.58−0.83)42437669.811.000.92/2.051.20/1.01/0.800.00
     Observer B0.68 (0.55−0.81)47.981.000.91/1.931.19/1.02/0.8211.89
    Left RD (mean)
     Observer A0.68 (0.55−0.81)128.061.000.91/1.921.18/1.01/0.8211.57
     Observer B0.68 (0.54−0.81)46.621.000.91/1.871.18/1.01/0.8226.58
    Volume
     Left0.67 (0.54−0.81)NA1.000.91/1.951.18/1.01/0.82543.73
     Right0.68 (0.55−0.81)NA1.000.91/1.721.17/1.01/0.824849.30
    • Note:—AUC indicates area under the receiver operating characteristic curve; MMSE, Mini-Mental State Examination; ADAS-Cog, Assessment Scale–Cognitive Subscale; RBMT, Rivermead Behavioral Memory Test; NA, not applicable.

    • ↵a The data in parentheses are 95% confidence intervals.

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Imaging Biomarker for Early-Stage Alzheimer Disease: Utility of Hippocampal Histogram Analysis of Diffusion Metrics
Hiroto Takahashi, Yoichi Takami, Shuko Takeda, Naoki Hayakawa, Tsuneo Nakajima, Yasushi Takeya, Chisato Matsuo-Hagiyama, Atsuko Arisawa, Hiromi Rakugi, Noriyuki Tomiyama
American Journal of Neuroradiology Feb 2024, DOI: 10.3174/ajnr.A8106
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Hiroto Takahashi, Yoichi Takami, Shuko Takeda, Naoki Hayakawa, Tsuneo Nakajima, Yasushi Takeya, Chisato Matsuo-Hagiyama, Atsuko Arisawa, Hiromi Rakugi, Noriyuki Tomiyama
Imaging Biomarker for Early-Stage Alzheimer Disease: Utility of Hippocampal Histogram Analysis of Diffusion Metrics
American Journal of Neuroradiology Feb 2024, DOI: 10.3174/ajnr.A8106

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