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Research ArticleEXTRACRANIAL VASCULAR
Open Access

MR Elastography Can Be Used to Measure Brain Stiffness Changes as a Result of Altered Cranial Venous Drainage During Jugular Compression

A. Hatt, S. Cheng, K. Tan, R. Sinkus and L.E. Bilston
American Journal of Neuroradiology October 2015, 36 (10) 1971-1977; DOI: https://doi.org/10.3174/ajnr.A4361
A. Hatt
aFrom Neuroscience Research Australia (A.H., S.C., K.T., L.E.B.), Randwick, New South Wales, Australia
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S. Cheng
aFrom Neuroscience Research Australia (A.H., S.C., K.T., L.E.B.), Randwick, New South Wales, Australia
bSchool of Mechanical Engineering (S.C.), Macquarie University, North Ryde, New South Wales, Australia
cSchool of Medical Sciences (S.C.)
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K. Tan
aFrom Neuroscience Research Australia (A.H., S.C., K.T., L.E.B.), Randwick, New South Wales, Australia
dGraduate School of Biomedical Engineering (K.T.), University of New South Wales, Kensington, New South Wales, Australia
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R. Sinkus
eBritish Heart Foundation Centre of Excellence (R.S.), Division of Imaging Sciences and Biomedical Engineering, King's College London, King's Health Partners, St. Thomas' Hospital, London, United Kingdom
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L.E. Bilston
aFrom Neuroscience Research Australia (A.H., S.C., K.T., L.E.B.), Randwick, New South Wales, Australia
fPrince of Wales Clinical School (L.E.B.), University of New South Wales, Randwick, New South Wales, Australia.
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    Fig 1.

    A, Sagittal view of imaging planes for the MRE study within and just above the ventricles, phase-contrast MR imaging CSF flow study of the cerebral aqueduct, and phase-contrast MR imaging flow study of the blood flow in the neck vessels at the level of the compression. The arrows denote the position of neck wrap. B, Images of neck vessels with and without the neck wrap, showing the reduction in internal jugular vein area. Internal jugular veins are indicated by white arrows.

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    Fig 2.

    Group mean flow waveforms for internal jugular vein flow (A) and carotid and vertebral artery flow (B); and group mean CSF velocity waveforms through the cerebral aqueduct (C). Venous flow-rate peaks are suppressed with jugular compression; however, arterial flow waveforms are unaffected. Maximal caudally directed velocity of the CSF in the aqueduct increases with jugular compression.

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    Fig 3.

    ROI and sample viscoelastic maps. A, Sample high-resolution anatomic image shows the ROI (yellow line). Viscoelastic property maps for G′ (B) and G″ (C) in kilopascals. In the viscoelastic maps, the ventricles and large sulci have very low (near zero) shear moduli, indicating that they are filled with CSF, which has waterlike properties. Stiffer tissue is indicated by warmer colors, as indicated by the color bar (right).

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    Fig 4.

    A, Individual subject change in G′ in unrestricted and jugular compression conditions for all subjects. B, Cerebral aqueduct CSF velocity waveforms for a single subject are depicted by the black line in A. In this subject, the 17% increase in G′ with jugular compression was related to a 61% increase in the maximal caudal CSF velocity and an 11% longer caudal-flow duration.

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    Fig 5.

    The relationship between shear moduli and the percentage of jugular vein flow with the cervical wrap in place. Storage modulus (G′, left) and loss modulus (G″, right). Error bars are standard error of the mean in both panels. Both storage and loss moduli are significantly correlated with the percentage of jugular vein flow with the cervical wrap in place (P < .05).

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    Table 1:

    Blood flow parameters

    Internal Jugular Vein FlowArterial Flow
    Unrestricted FlowJugular CompressionUnrestricted FlowJugular Compression
    Mean vessel area (cm2)
        Mean1.17 ± 0.540.70 ± 0.351.0 ± 0.770.97 ± 0.68
        Range0.40–2.180.29–1.41−0.99–1.53−0.76–1.56
        t testt = 3.56, P = .005at = 0.51, P = .604
    Mean flow rate (mL/min) (caudal flow for venous flow, cranial for arterial)
        Mean572.2 ± 219.7460.8 ± 202.4814.7 ± 221.9815.3 ± 290.6
        Range153.8–862.2135–726.4268–989.2127.7–1070
        t testt = 2.85, P = .008a−0.01, P = .989
    Flow-rate amplitude (mL/min)
        Mean974.1 ± 523.6382.6 ± 312.71803.8 ± 490.11720.6 ± 688.4
        Range198.5–1838.856.8–1069.0601.4–2290.2282.8–2721.4
        t testt = 3.75, P = .002at = 0.58, P = .558
    • ↵a P < .05, paired t test.

    • View popup
    Table 2:

    PJVF values for subjects

    PJVF
    Unrestricted FlowJugular Compression
    Subject 197.2%53.0%
    Subject 284.1%70.6%
    Subject 382.1%81.5%
    Subject 476.8%69.5%
    Subject 574.2%44.3%
    Subject 661.2%27.0%
    Subject 759.8%63.8%
    Subject 859.3%60.0%
    Subject 917.9%13.7%
    Mean68.1 ± 22.7%53.7 ± 21.9%
    t testt = 2.33, P = .019a
    Predominantly jugular flow (between 50% and 100%)
        Subjects8/96/9
    Predominantly nonjugular flow (<50%)
        Subjects1/93/9
    • ↵a P < .05, paired t test.

    • View popup
    Table 3:

    CSF velocity parameters

    Aqueductal Flow
    Unrestricted FlowJugular Compression
    Maximum caudal velocity (cm/s)
        Mean1.18 ± 0.331.53 ± 0.42
        Range0.81–1.851.04–2.36
        t testt = −4.96, P = .0004a
    Maximum cranial velocity (cm/s)
        Mean1.38 ± 0.571.62 ± 0.62
        Range0.73–2.470.66–2.48
         t testt = 1.58, P = .066
    Duration of caudally directed flow (% cardiac cycle)
        Mean49.9 ± 5.2%51.4 ± 5.3%
        Range40.7%–57.7%42.1%–61.7%
        t testt = −1.0, P = .160
    • ↵a P < .05, paired t test.

    • View popup
    Table 4:

    Elastic (G′) and viscous (G″) mechanical properties of brain tissue

    Unrestricted FlowJugular Compression
    G′ (kPa)
        Mean0.691 ± 0.0670.688 ± 0.065
        Range0.567–0.8050.606–0.798
        t testt = 0.17, P = .436
    G″ (kPa)
        Mean0.587 ± 0.0520.585 ± 0.046
        Range0.482–0.6620.531–0.645
        t testt = 0.23, P = .413
    • View popup
    Table 5:

    Linear regression coefficients for the relationships between PJVF and G′ and G″ with unrestricted flow and with jugular compression, and change in mean G′, G″, and maximal caudal CSF velocity

    R2P
    G′ and PJVF, unrestricted flow0.136.330
    G′ and PJVF, jugular compression0.475.040a
    G″ and PJVF, unrestricted flow0.151.301
    G″ and PJVF, jugular compression0.449.048a
    % Change G′ and % change in max. caudal CSF velocity0.412.063
    % Change G″ and % change in max. caudal CSF velocity0.171.268
    • Note:—max. indicates maximum.

    • ↵a P < .05, paired t test.

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American Journal of Neuroradiology: 36 (10)
American Journal of Neuroradiology
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1 Oct 2015
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Cite this article
A. Hatt, S. Cheng, K. Tan, R. Sinkus, L.E. Bilston
MR Elastography Can Be Used to Measure Brain Stiffness Changes as a Result of Altered Cranial Venous Drainage During Jugular Compression
American Journal of Neuroradiology Oct 2015, 36 (10) 1971-1977; DOI: 10.3174/ajnr.A4361

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MR Elastography Can Be Used to Measure Brain Stiffness Changes as a Result of Altered Cranial Venous Drainage During Jugular Compression
A. Hatt, S. Cheng, K. Tan, R. Sinkus, L.E. Bilston
American Journal of Neuroradiology Oct 2015, 36 (10) 1971-1977; DOI: 10.3174/ajnr.A4361
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