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Research ArticlePediatric Neuroimaging
Open Access

Exploratory Multisite MR Spectroscopic Imaging Shows White Matter Neuroaxonal Loss Associated with Complications of Type 1 Diabetes in Children

L.Y. Cai, C. Tanase, A.W. Anderson, N.J. Patel, C.A. Lee, R.S. Jones, L.M. LeStourgeon, A. Mahon, I. Taki, J. Juvera, S. Pruthi, K. Gwal, A. Ozturk, H. Kang, A. Rewers, M.J. Rewers, G.T. Alonso, N. Glaser, S. Ghetti, S.S. Jaser, B.A. Landman and L.C. Jordan
American Journal of Neuroradiology June 2023, DOI: https://doi.org/10.3174/ajnr.A7895
L.Y. Cai
aFrom the Department of Biomedical Engineering (L.Y.C., A.W.A., B.A.L.)
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C. Tanase
dDepartments of Psychiatry and Behavioral Sciences (C.T.)
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A.W. Anderson
aFrom the Department of Biomedical Engineering (L.Y.C., A.W.A., B.A.L.)
bVanderbilt University Institute of Imaging Science (A.W.A., B.A.L.)
fDepartments of Radiology and Radiological Sciences (A.W.A., S.P., B.A.L.)
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N.J. Patel
gPediatrics (N.J.P., R.S.J., S.S.J., L.C.J.)
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C.A. Lee
hNeurology (C.A.L., L.C.J.)
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R.S. Jones
gPediatrics (N.J.P., R.S.J., S.S.J., L.C.J.)
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L.M. LeStourgeon
iMedicine (L.M.L.)
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A. Mahon
ePsychology (A.M., S.G.), University of California, Davis, Davis, California
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  • ORCID record for A. Mahon
I. Taki
kDepartment of Pediatrics (I.T., A.R., M.J.R.)
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J. Juvera
mDepartment of Psychiatry (J.J.), University of Colorado Anschutz Medical Campus, Aurora, Colorado
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S. Pruthi
fDepartments of Radiology and Radiological Sciences (A.W.A., S.P., B.A.L.)
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K. Gwal
nDepartments of Radiology (K.G., A.O.)
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A. Ozturk
nDepartments of Radiology (K.G., A.O.)
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H. Kang
jBiostatistics (H.K.), Vanderbilt University Medical Center, Nashville, Tennessee
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A. Rewers
kDepartment of Pediatrics (I.T., A.R., M.J.R.)
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M.J. Rewers
kDepartment of Pediatrics (I.T., A.R., M.J.R.)
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G.T. Alonso
lBarbara Davis Center (G.T.A.)
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N. Glaser
oPediatrics (N.G.), University of California Davis Health, University of California Davis School of Medicine, Sacramento, California
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S. Ghetti
ePsychology (A.M., S.G.), University of California, Davis, Davis, California
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S.S. Jaser
gPediatrics (N.J.P., R.S.J., S.S.J., L.C.J.)
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B.A. Landman
aFrom the Department of Biomedical Engineering (L.Y.C., A.W.A., B.A.L.)
bVanderbilt University Institute of Imaging Science (A.W.A., B.A.L.)
cDepartment of Electrical and Computer Engineering (B.A.L.), Vanderbilt University, Nashville, Tennessee
fDepartments of Radiology and Radiological Sciences (A.W.A., S.P., B.A.L.)
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L.C. Jordan
gPediatrics (N.J.P., R.S.J., S.S.J., L.C.J.)
hNeurology (C.A.L., L.C.J.)
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  • FIG 1.
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    FIG 1.

    Illustrated MRSI workflow. After acquiring 2D MRSI and an associated T1WI-based segmentation, one spectrum for each region was generated by combining the spectra for all overlapping voxels in a weighted average based on overlap contribution (Equation). The regionally-weighted spectra were subsequently fit using LCModel to compute metabolite peaks, resulting in one metabolite ratio computed per participant per region. Of note, the pictured MRSI grid is provided only for illustrative purposes and does not represent collected data.

  • FIG 2.
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    FIG 2.

    Maps of weights used to compute weighted average spectra for WM and deep GM in a representative participant. Each voxel is colored to represent its percent contribution to the tissue-weighted spectra as well as the corresponding voxel-wise volume fraction in parentheses.

  • FIG 3.
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    FIG 3.

    Mean regionally weighted spectra with 95% confidence intervals across participants from 0.2 to 4.0 ppm. Spectra were extracted for each region for each participant from LCModel and plotted after baseline subtraction. a.u. indicates arbitrary units.

  • FIG 4.
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    FIG 4.

    Differences in NAA/Cr in T1D by region. A, The uncalibrated NAA/Cr ratios from the regionally weighted spectra are shown across participants. B, P values of statistical comparisons between WM and deep GM as a whole and the individual deep nuclei. C, P values of contralateral comparisons in deep GM nuclei. D, P values of ipsilateral comparisons in deep GM nuclei. Statistical significance between regions was determined with pair-wise Wilcoxon signed-rank tests after false discovery rate correction (en dash indicates not tested; ns, not significant; single asterisk, P < .05; double asterisks, P < .005; triple asterisks, P < .0005). RC indicates right caudate; RBG, right basal ganglia; RTH, right thalamus; LC, left caudate; LBG, left basal ganglia; LTH, left thalamus; DGM, deep GM.

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    FIG 5.

    Associations of NAA/Cr in WM with T1D complications. The calibrated NAA/Cr ratios in WM are shown plotted against HbA1c, DKA status, and their interaction. Data points are colored by site with the symbol denoting the participant’s DKA status.

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    Table 1:

    Cohort demographics by site

    Site ASite BSite COverall
    Sample size (No.)1011425
    Age (yr) (mean)10.6 (SD, 1.1)10.5 (SD, 2.7)8.5 (SD, 1.3)10.2 (SD, 2.0)
    Sex, female (No.)7 (70%)5 (45%)3 (75%)15 (60%)
    Duration (yr) (mean)2.6 (SD, 2.3)4.6 (SD, 3.3)0.3 (SD, 0.1)3.1 (SD, 3.0)
    HbA1c (%) (mean)9.5 (SD, 3.2)8.5 (SD, 1.9)6.2 (SD, 0.9)8.5 (SD, 2.6)
    DKA at onset (No.)5 (50%)9 (82%)0 (0%)14 (56%)
    Race (No)
     White7 (70%)8 (73%)4 (100%)19 (76%)
     Black/African American2 (20%)1 (9%)0 (0%)3 (12%)
     Multiracial (black/white)0 (0%)1 (9%)0 (0%)1 (4%)
     Other1 (10%)1 (9%)0 (0%)2 (8%)
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    Table 2:

    Effect sizes, Akaike Information Criterion, and adjusted R2 for forward model selection of NAA/Cr in WM and deep GM with T1D covariates

    TissueHbA1cDKAHbA1c x DKAAgeSexDurationAkaikeaR2
    WM –0.086a–––––17.5810.291
     –0.080b–0.095––––19.0830.273
     –0.171a,c–1.142b,c0.130b,c–––15.373c0.394c
     –0.169a–1.156b0.131b–0.009––17.2980.365
     –0.187a–1.209b0.141b–0.0010.175–17.0860.389
     –0.187a–1.267b0.144b–0.0050.1890.01218.7990.362
    Deep GM –0.016c––––––29.356c0.061c
     –0.0180.034–––––27.7850.034
     –0.027–0.0650.012––––26.087–0.001
     –0.029–0.0430.0100.011–––24.800–0.023
     –0.027–0.0350.0090.010–0.018––22.922–0.075
     –0.028–0.0860.0110.007–0.0050.011–22.194–0.079
    • Note:—The en dash indicates that term was not included in model; aR2, adjusted R2.

    • ↵a P < .005.

    • ↵b P < .05.

    • ↵c Model with lowest Akaike Information Criterion.

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L.Y. Cai, C. Tanase, A.W. Anderson, N.J. Patel, C.A. Lee, R.S. Jones, L.M. LeStourgeon, A. Mahon, I. Taki, J. Juvera, S. Pruthi, K. Gwal, A. Ozturk, H. Kang, A. Rewers, M.J. Rewers, G.T. Alonso, N. Glaser, S. Ghetti, S.S. Jaser, B.A. Landman, L.C. Jordan
Exploratory Multisite MR Spectroscopic Imaging Shows White Matter Neuroaxonal Loss Associated with Complications of Type 1 Diabetes in Children
American Journal of Neuroradiology Jun 2023, DOI: 10.3174/ajnr.A7895

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Exploratory Multisite MR Spectroscopic Imaging Shows White Matter Neuroaxonal Loss Associated with Complications of Type 1 Diabetes in Children
L.Y. Cai, C. Tanase, A.W. Anderson, N.J. Patel, C.A. Lee, R.S. Jones, L.M. LeStourgeon, A. Mahon, I. Taki, J. Juvera, S. Pruthi, K. Gwal, A. Ozturk, H. Kang, A. Rewers, M.J. Rewers, G.T. Alonso, N. Glaser, S. Ghetti, S.S. Jaser, B.A. Landman, L.C. Jordan
American Journal of Neuroradiology Jun 2023, DOI: 10.3174/ajnr.A7895
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