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Research ArticleHead & Neck
Open Access

Altered Blood Flow in the Ophthalmic and Internal Carotid Arteries in Patients with Age-Related Macular Degeneration Measured Using Noncontrast MR Angiography at 7T

M.L. Hibert, Y.I. Chen, N. Ohringer, W.J. Feuer, N.K. Waheed, J.S. Heier, M.W. Calhoun, P.J. Rosenfeld and J.R. Polimeni
American Journal of Neuroradiology September 2021, 42 (9) 1653-1660; DOI: https://doi.org/10.3174/ajnr.A7187
M.L. Hibert
aFrom the Athinoula A. Martinos Center for Biomedical Imaging (M.L.H., Y.I.C., N. O., J.R.P.), Massachusetts General Hospital, Charlestown, Massachusetts
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Y.I. Chen
aFrom the Athinoula A. Martinos Center for Biomedical Imaging (M.L.H., Y.I.C., N. O., J.R.P.), Massachusetts General Hospital, Charlestown, Massachusetts
bDepartment of Radiology (Y.I.C., J.R.P.), Harvard Medical School, Boston, Massachusetts
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N. Ohringer
aFrom the Athinoula A. Martinos Center for Biomedical Imaging (M.L.H., Y.I.C., N. O., J.R.P.), Massachusetts General Hospital, Charlestown, Massachusetts
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W.J. Feuer
cDepartment of Ophthalmology (W.J.F., P.J.R.), Bascom Palmer Eye Institute, University of Miami Miller School of Medicine, Miami, Florida
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N.K. Waheed
dNew England Eye Center (N.K.W.), Tufts Medical Center, Boston, Massachusetts
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J.S. Heier
eOphthalmic Consultants of Boston (J.S.H.), Boston, Massachusetts
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M.W. Calhoun
fOcuDyne Inc (M.W.C.), Roseville, Minnesota
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P.J. Rosenfeld
cDepartment of Ophthalmology (W.J.F., P.J.R.), Bascom Palmer Eye Institute, University of Miami Miller School of Medicine, Miami, Florida
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J.R. Polimeni
aFrom the Athinoula A. Martinos Center for Biomedical Imaging (M.L.H., Y.I.C., N. O., J.R.P.), Massachusetts General Hospital, Charlestown, Massachusetts
bDepartment of Radiology (Y.I.C., J.R.P.), Harvard Medical School, Boston, Massachusetts
gHarvard-Massachusetts Institute of Technology Division of Health Sciences and Technology (J.R.P.), Massachusetts Institute of Technology, Cambridge, Massachusetts
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  • FIG 1.
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    FIG 1.

    Positioning of PC-MRA slices using the 3D-TOF-MRA data as an anatomic guide. A, Red lines depict cross-sections of the triple-oblique positioning and location of PC-MRA slices centered on and perpendicular to each OA (green arrows), identified from the reference 3D-TOF image. The OA cross-section can be visualized in the center of the magnitude (B and C) and phase (D and E) images from a PC-MRA scan (yellow box represents an enlarged region from B and D in C and E, respectively).

  • FIG 2.
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    FIG 2.

    Analysis procedure for correcting EC bias and defining the vessel ROI. A, A PC-MRA magnitude image is used to place a 12-mm-diameter ROI for EC correction in vessel-free tissue adjacent to the vessel ROI (blue). The red line in the inset TOF image indicates the PC-MRA slice position. The vessel ROI (yellow) is shown within the yellow box, which depicts the region enlarged in B and C. Enlarged PC-MRA magnitude images show the vessel cross-section alone (B) and with the vessel ROI superimposed (C). D, Time-series of EC-corrected flow data in units of centimeters/second from 1 example PC-MRA acquisition with a single VENC value in 1 subject.

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    FIG 3.

    Boxplots of unnormalized flow velocities (A and B) and volumetric flow rates (C and D) in the OAs (A and C) and ICAs (B and D). Vessels were divided into 4 groups: healthy controls, early AMD, intermediate AMD, and late AMD. The asterisk signifies P < .05 compared with controls.

  • FIG 4.
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    FIG 4.

    Linear trend test plot, which demonstrates that the rate of decline in OA volumetric flow with disease progression is statistically significant.

  • FIG 5.
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    FIG 5.

    Boxplots of flow velocity (A) and volumetric flow (B) in the OA normalized to upstream ICA flow rates. Normalized flow values represent the OA flow as a ratio of ICA flow. Vessels are divided into 4 groups: healthy controls, early AMD, intermediate AMD, and late AMD. The asterisk signifies P < .05 compared with controls.

  • FIG 6.
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    FIG 6.

    Resistance indices for the OA (A) and ICA (B). Vessels are divided into 4 groups: healthy controls, early AMD, intermediate AMD, and late AMD. The asterisk signifies P < .05 compared with controls.

Tables

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  • Summary of vessel diameter and blood flow measures stratified by disease stagea

    Control (Mean) (SD) (n = 20 OA, 24 ICA)Early AMD (Mean) (SD) (n = 9 OA, 15 ICA)Interm. AMD(Mean) (SD) (n = 7 OA, 8 ICA)Late AMD (Mean) (SD) (n = 12 OA, 17 ICA)All AMD (Mean) (SD) (n = 28 OA, 40 ICA)
    OA diameter (mm)1.1 (0.19)0.9 (0.25)P = .111.0 (0.26)P = .420.8 (0.25)P < .01b0.9 (0.26)P < .01b
    OA volume flow (mL/min)7.0 (3.0)6.5 (4.2)P = .745.6 (3.1)P = .373.8 (1.8)P < .01b5.1 (3.2)P = .07
    OA flow velocity (cm/s)c13.1 (4.0)16.0 (4.5)P < .01b11.9 (4.3)P = .9115.0 (5.7)P = .03b14.6 (5.1)P = .02b
    OA RI0.70 (0.10)0.82 (0.10)P < .01b0.81 (0.06)P < .01b0.80 (0.07)P < .01b0.81 (0.08)P < .01b
    ICA diameter (mm)4.3 (0.51)4.2 (0.52)P = .384.6 (0.63)P = .474.2 (0.44)P = .554.3 (0.52)P = .67
    ICA volume flow (mL/min)c163.1 (44.8)154.3 (44.2)P = .98167.0 (23.4)P = .49166.6 (27.7)P = .19162.2 (33.8)P = .46
    ICA flow velocity (cm/s)c18.3 (3.5)18.7 (3.7)P = .0717.8 (4.5)P = .5820.6 (5.2)P < .01b19.4 (4.6)P < .01b
    ICA RI0.61 (0.09)0.66 (0.09)P = .180.70 (0.04)P < .01b0.65 (0.11)P = .290.67 (0.09)P = .07
    • Note:—RI indicates resistance index; Interm., intermediate.

    • a Values represent group mean and group SD, and reported P values indicate significance relative to controls based on a GEE analysis followed by post hoc least significant difference comparisons between disease groups and controls. The sample size for ophthalmic artery measurements was 48 hemisphere measurements from 30 subjects. The sample size for the ICA measurements was 64 hemispheres of 33 subjects.

    • ↵b Tests that were significant at the P < .05 level (uncorrected).

    • ↵c Adjusted for age, which was statistically significant (P < .05) in the GEE model.

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American Journal of Neuroradiology: 42 (9)
American Journal of Neuroradiology
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1 Sep 2021
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Altered Blood Flow in the Ophthalmic and Internal Carotid Arteries in Patients with Age-Related Macular Degeneration Measured Using Noncontrast MR Angiography at 7T
M.L. Hibert, Y.I. Chen, N. Ohringer, W.J. Feuer, N.K. Waheed, J.S. Heier, M.W. Calhoun, P.J. Rosenfeld, J.R. Polimeni
American Journal of Neuroradiology Sep 2021, 42 (9) 1653-1660; DOI: 10.3174/ajnr.A7187

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Altered Blood Flow in the Ophthalmic and Internal Carotid Arteries in Patients with Age-Related Macular Degeneration Measured Using Noncontrast MR Angiography at 7T
M.L. Hibert, Y.I. Chen, N. Ohringer, W.J. Feuer, N.K. Waheed, J.S. Heier, M.W. Calhoun, P.J. Rosenfeld, J.R. Polimeni
American Journal of Neuroradiology Sep 2021, 42 (9) 1653-1660; DOI: 10.3174/ajnr.A7187
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