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Research ArticleBrain
Open Access

Effect of Age on MRI Phase Behavior in the Subcortical Deep Gray Matter of Healthy Individuals

J. Hagemeier, M.G. Dwyer, N. Bergsland, F. Schweser, C.R. Magnano, M. Heininen-Brown, D.P. Ramasamy, E. Carl, C. Kennedy, R. Melia, P. Polak, A. Deistung, J.J.G. Geurts, J.R. Reichenbach and R. Zivadinov
American Journal of Neuroradiology November 2013, 34 (11) 2144-2151; DOI: https://doi.org/10.3174/ajnr.A3569
J. Hagemeier
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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M.G. Dwyer
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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N. Bergsland
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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F. Schweser
bMedical Physics Group (F.S., A.D., J.R.R.), Institute of Diagnostic and Interventional Radiology I, Jena University Hospital–Friedrich Schiller University, Jena, Germany
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C.R. Magnano
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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M. Heininen-Brown
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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D.P. Ramasamy
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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E. Carl
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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C. Kennedy
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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R. Melia
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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P. Polak
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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A. Deistung
bMedical Physics Group (F.S., A.D., J.R.R.), Institute of Diagnostic and Interventional Radiology I, Jena University Hospital–Friedrich Schiller University, Jena, Germany
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J.J.G. Geurts
cDepartment of Anatomy and Neurosciences (J.J.G.G.), Section of Clinical Neuroscience, VU University Medical Center, Amsterdam, The Netherlands.
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J.R. Reichenbach
bMedical Physics Group (F.S., A.D., J.R.R.), Institute of Diagnostic and Interventional Radiology I, Jena University Hospital–Friedrich Schiller University, Jena, Germany
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R. Zivadinov
aFrom the Buffalo Neuroimaging Analysis Center (J.H., M.G.D., N.B., C.R.M., M.H.-B., D.P.R., E.C., C.K., R.M., P.P., R.Z.), Department of Neurology, University at Buffalo, Buffalo, New York
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  • Fig 1.
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    Fig 1.

    Phase maps (upper row) and thresholded low-phase voxels used in mean phase of low-phase voxel (MP-LPV) calculation (bottom row) of subcortical deep gray matter structures. MP-LPV was determined by thresholding the phase images to retain only those voxels with phase values lower than 2 standard deviations below reference group. Upper and lower rows show the same subjects, and each column contains a representative subject from each age group (left to right, <25 years, 25–39 years, 40–55 years, >55 years).

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    Fig 2.

    Scatterplots showing significant interaction effects between sex and the mean phase of low-phase voxels (MP-LPV) of the putamen and substantia nigra.

Tables

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    Table 1:

    Demographic characteristics and global volumetric MRI measures of study participants

    TotalMaleFemaleP
    n (%)21089 (42.4)121 (57.6)
    Age (SD) median39.8 (15.5) 4138 (16.1) 3841.1 (14.9) 44.202
    Race, n (%) of available cases
        White139 (87.4)58 (87.9)81 (87.1).617
        African American13 (8.2)5 (7.6)8 (8.6)
        Other7 (4.4)3 (4.5)4 (4.3)
        Education, n (%) of available cases
        No high school15 (9.7)7 (11.3)8 (8.7).893
        High school24 (15.6)11 (17.7)13 (14.1)
        Some college32 (20.8)14 (22.6)18 (19.6)
        Associate/technical22 (14.3)7 (11.3)15 (16.3)
        Bachelor level36 (23.4)12 (19.4)24 (26.1)
        Graduate level23 (14.9)10 (16.1)13 (14.1)
        Postgraduate2 (1.3)1 (1.6)1 (1.1)
    MRI volumes in cm3, mean (SD)
        WM hyperintensities1.26 (4.47)1.74 (6.50)0.87 (1.29).160
        GM791.93 (65.56)787.64 (69.36)795.02 (62.81).525
        Cortical GM644.30 (56.33)637.10 (62.11)649.56 (51.36).181
        WM761.95 (41.39)771.66 (39.57)754.97 (41.41).008
        Lateral ventricles31.66 (12.70)33.46 (13.36)30.35 (12.07).136
    • Note:—Differences between men and women were assessed by means of the χ2 test (race and education) and Student t test (age and normalized volumes).

    • View popup
    Table 2:

    Sex differences of mean phase, mean phase of low-phase voxels, and normalized volume values of subcortical deep gray matter structures

    Mean PhaseMP-LPVNormalized Volume
    Male (n = 89)Female (n = 121)PMale (n = 89)Female (n = 121)PMale (n = 89)Female (n = 121)P
    Total SDGM−.012 (.014)−.016 (.014).036−.144 (.022)−.149 (.027).57349.209 (5.474)44.442 (3.551)<.001
    Caudate−.054 (.017)−.064 (.018).001−.170 (.016)−.167 (.014).5257.398 (1.079)6.832 (.890)<.001
    Putamen−.018 (.028)−.027 (.029).028−.175 (.039)−.183 (.047).48710.471 (1.386)9.426 (.914)<.001
    Globus pallidus−.016 (.025)−.015 (.024).643−.184 (.033)−.183 (.042).3483.809 (.442)3.431 (.399)<.001
    Thalamus.005 (.008).003 (.009).210−.095 (.015)−.091 (.013).15716.474 (1.923)14.661 (1.188)<.001
    Pulvinar−.042 (.030)−.042 (.028).657−.139 (.017)−.140 (.018).689.456 (.092).419 (.090).010
    Hippocampus.024 (.032).031 (.039).073−.161 (.044)−.165 (.049).8227.559 (.956)6.981 (.817)<.001
    Amygdala.011 (.039)−.007 (.066).086−.214 (.051)−.210 (.075).0862.634 (.424)2.326 (.307)<.001
    Accumbens−.179 (.140)−.230 (.163).035−.744 (.203)−.80 (.252).298.865 (.199).784 (.189).006
    Red nucleus−.050 (.057)−.059 (.051).331−.238 (.027)−.232 (.026).225.179 (.023).162 (.022)<.001
    Substantia nigra−.097 (.056)−.096 (.057).765−.305 (.039)−.308 (.041).574.305 (.048).282 (.053).005
    • Note:—Results are shown as mean (standard deviation); volume measurements are expressed in cubic centimeters. Mean phase and mean phase of low-phase tissue (MP-LPV) measurements are expressed in radians. Statistical analyses were carried out by use of independent-samples t test and Mann-Whitney U test.

    • View popup
    Table 3:

    Linear regression analyses assessing the association between age and mean phase, mean phase of low-phase tissue, and normalized volumes, adjusted for sex

    Mean phaseaMP-LPVaNormalized Volume
    βPβPβP
    Total SDGM−.102.057−.255<.001−.245<.001
    Caudate−.102.068−.350<.001−.247<.001
    Putamen−.208<.001−.193<.001−.239<.001
    lobus pallidus.210<.001−.273<.001.049.352
    Thalamus−.178<.001−.521<.001−.299<.001
    Pulvinar nucleus−.384<.001−.340<.001−.105.059
    Hippocampus−.027.645.033.589−.075.163
    Amygdala.039.525−.029.631.069.197
    Accumbens−.051.376.112.043−.271<.001
    Red nucleus−.301<.001−.252<.001−.195<.001
    Substantia nigra−.207.006−.256<.001.023.687
    • ↵a Adjusted for the effects of normalized volume.

    • View popup
    Table 4:

    Proportion of structural low-phase voxels versus structural normalized volume within age groups, adjusted for sex

    Age (years)P
    <25 n = 4325–39 n = 5640–55 n = 72≥55 n = 39
    Total SDGM.29 (.04).32 (.03).34 (.04).35 (.04)<.001
    Caudate.27 (.09).33 (.08).36 (.07).35 (.08)<.001
    Putamen.17 (.08).26 (.06).33 (.07).32 (.09)<.001
    Globus pallidus.42 (.07).40 (.06).38 (.06).35 (.06)<.001
    Thalamus.40 (.03).43 (.03).44 (.04).43 (.04)<.001
    Pulvinar nucleus.11 (.08).24 (.16).28 (.15).29 (.14)<.001
    Hippocampus.15 (.08).19 (.09).18 (.07).18 (.07).319
    Amygdala.17 (.14).18 (.10).17 (.10).16 (.08).738
    Accumbens.15 (.14).14 (.14).12 (.13).13 (.16).703
    Red nucleus.05 (.05).13 (.12).21 (.13).17 (.11)<.001
    Substantia nigra.17 (.11).23 (.11).27 (.11).24 (.14).002
    • General linear modeling comparing the proportion of structural low-phase voxels versus structural normalized volume between age groups. Results are presented as mean (standard deviation).

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J. Hagemeier, M.G. Dwyer, N. Bergsland, F. Schweser, C.R. Magnano, M. Heininen-Brown, D.P. Ramasamy, E. Carl, C. Kennedy, R. Melia, P. Polak, A. Deistung, J.J.G. Geurts, J.R. Reichenbach, R. Zivadinov
Effect of Age on MRI Phase Behavior in the Subcortical Deep Gray Matter of Healthy Individuals
American Journal of Neuroradiology Nov 2013, 34 (11) 2144-2151; DOI: 10.3174/ajnr.A3569

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Effect of Age on MRI Phase Behavior in the Subcortical Deep Gray Matter of Healthy Individuals
J. Hagemeier, M.G. Dwyer, N. Bergsland, F. Schweser, C.R. Magnano, M. Heininen-Brown, D.P. Ramasamy, E. Carl, C. Kennedy, R. Melia, P. Polak, A. Deistung, J.J.G. Geurts, J.R. Reichenbach, R. Zivadinov
American Journal of Neuroradiology Nov 2013, 34 (11) 2144-2151; DOI: 10.3174/ajnr.A3569
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