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Research ArticleAdult Brain
Open Access

The Brain Thermal Response as a Potential Neuroimaging Biomarker of Cerebrovascular Impairment

C.C. Fleischer, J. Wu, D. Qiu, S.-E. Park, F. Nahab and S. Dehkharghani
American Journal of Neuroradiology November 2017, 38 (11) 2044-2051; DOI: https://doi.org/10.3174/ajnr.A5380
C.C. Fleischer
aFrom the Department of Biomedical Engineering (C.C.F., S.-E.P.), Emory University and Georgia Institute of Technology, Atlanta, Georgia
bthe Departments of Radiology and Imaging Sciences (C.C.F., J.W., D.Q., S.D.)
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J. Wu
bthe Departments of Radiology and Imaging Sciences (C.C.F., J.W., D.Q., S.D.)
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D. Qiu
bthe Departments of Radiology and Imaging Sciences (C.C.F., J.W., D.Q., S.D.)
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S.-E. Park
aFrom the Department of Biomedical Engineering (C.C.F., S.-E.P.), Emory University and Georgia Institute of Technology, Atlanta, Georgia
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F. Nahab
cNeurology (F.N., S.D.)
dPediatrics (F.N.), Emory University School of Medicine, Atlanta, Georgia.
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S. Dehkharghani
bthe Departments of Radiology and Imaging Sciences (C.C.F., J.W., D.Q., S.D.)
cNeurology (F.N., S.D.)
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    Fig 1.

    Schematic of MR imaging scan protocol. ACZ was injected 5 minutes after the start of the BOLD sequence and data were acquired for ∼10 minutes post-injection. ASL and MRSI were acquired pre- and post-ACZ.

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    Fig 2.

    Representative CVR percentage augmentation maps calculated with BOLD and ASL, along with a BTR map overlaid on a T1-weighted image. Images are all from the same subject (a 32-year-old woman) with unilateral left MCA stenosis without infarction. The white grid overlay represents the MR thermometry grid derived from multivoxel spectroscopy analysis using the water-NAA chemical shift difference. Diffusion-weighted imaging demonstrates no evidence for acute infarction. Images are displayed in the radiologic convention. Impaired CVR in the left hemisphere is present in both BOLD and ASL, with a greater severity of impairment in ASL likely related to delay sensitivity and tag decay (see text). The BTR map demonstrates an asymmetric thermal response, with less brain cooling following vasodilatory stimulus in the diseased left hemisphere, indicated by lower and more positive BTR values and corresponding primarily to the areas of greatest impairment in the anterior and posterior MCA borderzone territories.

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    Fig 3.

    Voxelwise relationship of the BTR versus BOLD MR imaging signal augmentation following ACZ administration. The blue line and corresponding equation represent the fit of the raw data (circles) calculated with a mixed-effects model. A significant quadratic relationship between BTR and CVRBOLD was identified for all voxels, wherein an initially negative slope is observed at low CVRBOLD but a positive trend is observed for CVRBOLD augmentation upward of approximately 4% (see “Results” and “Discussion”; F, x2 = 57.5, P < .001; F, x = 74.1, P < .001).

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    Table 1:

    Patient characteristics

    Patient No.Age (years)SexPresentation and Diagnosis
    141FLeft-sided-predominate supraclinoid ICA stenosis
    261MLeft cervical ICA stenosis; aphasia
    339FRight-sided-predominate ICA stenosis; recurrent minor stroke
    432FLeft M1 stenosis; left monocular vision loss and recurrent right hemiparesis
    556MIntracranial ICA stenosis; recurrent TIA
    668FLeft ICA stenosis; recurrent left hemispheric TIA and borderzone ischemia
    733FRight-sided-predominate supraclinoid ICA stenosis; Moyamoya disease following STA-MCA bypass and recurrent TIA
    836FLeft M1 stenosis; recurrent left deep borderzone ischemia
    938FRight-sided-predominate intracranial stenosis; recurrent MCA infarctions
    1051FLeft ICA stenosis; recurrent TIA
    • Note:—STA indicates superficial temporal artery.

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    Table 2:

    Parameter estimates calculated with a mixed-effects model of BTR and baseline brain temperature as a function of CVR

    CVRCVR2Intercept
    CoefficientFdfaP ValueCoefficientFdfaP ValueCoefficientFdfaP Valueb
    BTR
        CVRBOLD−0.05274.11, 513<.0010.006857.51, 619<.0010.0316.01, 35.02
        CVRASL0.00181.21, 8.0.30––––−0.0692051, 3.8<.001
        CVRBOLD < 70c−0.09659.71, 97<.0010.02425.01, 128<.0010.0312.81, 11.12
        CVRBOLD ≥ 70c0.00705.51, 200.02––––−0.08146.01, 51<.001
        CVRASL < 30d0.00181.11, 7.4.33––––−0.068183.21, 69<.001
        CVRASL ≥ 30d0.001412.11, 47.001––––−0.1033.51, 44<.001
    Tpree (°C)
        CVRBOLD0.597.01, 598.008−0.1314.81, 630<.00137.548711, 27<.001
        CVRASL−0.0390.91, 7.3.39––––38.486551, 6.0<.001
        CVRBOLD < 70c2.119.51, 139<.001−0.6512.91, 150<.00137.118101, 17<.001
        CVRBOLD ≥ 70c−0.3810.71, 429.001––––39.045751, 28<.001
        CVRASL < 30d−0.0491.11, 6.8.34––––38.512,9531, 6.5<.001
        CVRASL ≥ 30d0.00260.011, 198.91––––37.510941, 27<.001
    • ↵a df calculated with the Satterthwaite approximation are reported as numerator, denominator.

    • ↵b P value represents the significance of a nonzero intercept.

    • ↵c CVRBOLD values thresholded to 70% of the subject-wise mean contralateral value.

    • ↵d CVRASL values thresholded to 30% augmentation.

    • ↵e Tpre is the baseline brain temperature.

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American Journal of Neuroradiology: 38 (11)
American Journal of Neuroradiology
Vol. 38, Issue 11
1 Nov 2017
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The Brain Thermal Response as a Potential Neuroimaging Biomarker of Cerebrovascular Impairment
C.C. Fleischer, J. Wu, D. Qiu, S.-E. Park, F. Nahab, S. Dehkharghani
American Journal of Neuroradiology Nov 2017, 38 (11) 2044-2051; DOI: 10.3174/ajnr.A5380

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The Brain Thermal Response as a Potential Neuroimaging Biomarker of Cerebrovascular Impairment
C.C. Fleischer, J. Wu, D. Qiu, S.-E. Park, F. Nahab, S. Dehkharghani
American Journal of Neuroradiology Nov 2017, 38 (11) 2044-2051; DOI: 10.3174/ajnr.A5380
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