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Research ArticleExtracranial Vascular
Open Access

Proximal Region of Carotid Atherosclerotic Plaque Shows More Intraplaque Hemorrhage: The Plaque at Risk Study

G.A.J.C. Crombag, M. Aizaz, F.H.B.M. Schreuder, F. Benali, D.H.K. van Dam-Nolen, M.I. Liem, C. Lucci, A.F. van der Steen, M.J.A.P. Daemen, W.H. Mess, A. van der Lugt, P.J. Nederkoorn, J. Hendrikse, P.A.M. Hofman, R.J. van Oostenbrugge, J.E. Wildberger and M.E. Kooi
American Journal of Neuroradiology February 2022, 43 (2) 265-271; DOI: https://doi.org/10.3174/ajnr.A7384
G.A.J.C. Crombag
aFrom the Departments of Radiology and Nuclear Medicine (G.A.J.C.C., M.A., F.B., P.A.M.H., J.E.W., M.E.K.)
dCARIM School for Cardiovascular Diseases (G.A.J.C.C., M.A., R.J.v.O., J.E.W., M.E.K.), Maastricht University, Maastricht, the Netherlands
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  • ORCID record for G.A.J.C. Crombag
M. Aizaz
aFrom the Departments of Radiology and Nuclear Medicine (G.A.J.C.C., M.A., F.B., P.A.M.H., J.E.W., M.E.K.)
dCARIM School for Cardiovascular Diseases (G.A.J.C.C., M.A., R.J.v.O., J.E.W., M.E.K.), Maastricht University, Maastricht, the Netherlands
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F.H.B.M. Schreuder
eDepartment of Neurology & Donders Institute for Brain Cognition & Behaviour (F.H.B.M.S.), Radboud University Medical Center, Nijmegen, the Netherlands
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F. Benali
aFrom the Departments of Radiology and Nuclear Medicine (G.A.J.C.C., M.A., F.B., P.A.M.H., J.E.W., M.E.K.)
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D.H.K. van Dam-Nolen
fDepartments of Radiology and Nuclear Medicine (D.H.K.v.D.-N., A.v.d.L.)
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M.I. Liem
hDepartments of Neurology (M.I.L., P.J.N.)
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C. Lucci
jDepartment of Radiology (C.L., J.H.), University Medical Center Utrecht, Utrecht, the Netherlands
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A.F. van der Steen
gBiomedical Engineering (A.F.v.d.S.), Erasmus University Medical Center, University Medical Center Rotterdam, Rotterdam, the Netherlands
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M.J.A.P. Daemen
iPathology (M.J.A.P.D.), Amsterdam University Medical Centres, University of Amsterdam, Amsterdam, the Netherlands
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W.H. Mess
bClinical Neurophysiology (W.H.M.)
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A. van der Lugt
fDepartments of Radiology and Nuclear Medicine (D.H.K.v.D.-N., A.v.d.L.)
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P.J. Nederkoorn
hDepartments of Neurology (M.I.L., P.J.N.)
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J. Hendrikse
jDepartment of Radiology (C.L., J.H.), University Medical Center Utrecht, Utrecht, the Netherlands
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P.A.M. Hofman
aFrom the Departments of Radiology and Nuclear Medicine (G.A.J.C.C., M.A., F.B., P.A.M.H., J.E.W., M.E.K.)
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R.J. van Oostenbrugge
dCARIM School for Cardiovascular Diseases (G.A.J.C.C., M.A., R.J.v.O., J.E.W., M.E.K.), Maastricht University, Maastricht, the Netherlands
cNeurology (R.J.v.O.), Maastricht University Medical Center, Maastricht, the Netherlands
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J.E. Wildberger
aFrom the Departments of Radiology and Nuclear Medicine (G.A.J.C.C., M.A., F.B., P.A.M.H., J.E.W., M.E.K.)
dCARIM School for Cardiovascular Diseases (G.A.J.C.C., M.A., R.J.v.O., J.E.W., M.E.K.), Maastricht University, Maastricht, the Netherlands
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M.E. Kooi
aFrom the Departments of Radiology and Nuclear Medicine (G.A.J.C.C., M.A., F.B., P.A.M.H., J.E.W., M.E.K.)
dCARIM School for Cardiovascular Diseases (G.A.J.C.C., M.A., R.J.v.O., J.E.W., M.E.K.), Maastricht University, Maastricht, the Netherlands
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    FIG 1.

    Transversal MR images of carotid plaque in the right carotid artery. We acquired the following MR images: precontrast T1-weighted QIR TSE (A), postcontrast T1-weighted QIR TSE (B), T1-weighted inversion recovery turbo field echo (C). D, The same image as in B, including the contours delineating intraplaque hemorrhage and the inner and outer vessel wall: white = lumen, gray = outer vessel wall, black = intraplaque hemorrhage. C, A hyperintense signal in the bulk of the plaque can be clearly observed, indicating the presence of intraplaque hemorrhage (black asterisk). B, An interruption of the signal enhancement adjoining the lumen can be observed, indicating a TRFC (white arrow).

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    FIG 2.

    A patient’s dataset acquired with an inversion recovery turbo field echo sequence. Delineation of the inner and outer vessel walls and IPH in every 2-mm-thick MR imaging section proximal and distal to the section with the narrowest lumen (0 mm). Gray outline = outer vessel wall, white outline = inner vessel wall, black outline= IPH, white arrow (−6 mm to +2 mm) = MR imaging slices in which the FC status is scored as thin or ruptured. The status of the FC was determined by using the postcontrast T1-weighted QIR TSE sequence. There is a larger volume of IPH at the proximal side of the section with the narrowest lumen (0 mm), and most of the slices with a TRFC cap are also located at the proximal side.

  • FIG 3.
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    FIG 3.

    A, Histogram showing significantly larger mean IPH areas in the proximal region of the plaque compared with the distal region. Mean IPH area percentages are shown for each section in relation to the smallest lumen. The white bar indicates the section with the narrowest lumen (distance = 0 mm), the bars on the left with the negative numbers are slices proximal (proximally), and the bars on the right with the positive numbers indicate the slices distal to the smallest lumen. Each section has a thickness of 2 mm. An asterisk indicates a statistically significant difference (P < .05) between the proximal and distal slices using a paired t test. B, Prevalence of a TRFC plotted for each section position with respect to the section with the smallest lumen (0). The bars on the left with the negative numbers are slices proximal, and the bars on the right with the positive numbers indicate the slices distal to the smallest lumen. An asterisk indicates a statistically significant difference (P < .05) between the proximal and distal slices using a McNemar test.

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    Table 1:

    Differences in mean IPH area (% of total vessel wall) between proximal and distal regions

    Longitudinal Distance from Section with Smallest Lumen (mm)No. of Slices Where Proximal and Distal Sections Are AvailableMean % IPH with Respect to Total Vessel Wall Area in the Proximal RegionMean % IPH with Respect to Total Vessel Wall Area in the Distal RegionP Value
    26614.4 (SD, 1.9)9.6 (SD, 2.1).040
    45914.7 (SD, 1.7)5.4 (SD, 1.8)<.001
    64511.1 (SD, 1.6)2.2 (SD, 1.3).001
    8397.5 (SD, 1.5)2.2 (SD, 1.5).056
    10345.0 (SD, 1.4)1.1 (SD, 1).077
    • View popup
    Table 2:

    Differences in prevalence of a TRFC between proximal and distal regions

    Longitudinal Distance from Section with Narrowest Lumen (mm)No. of Slices Where Proximal and Distal Sections Are AvailableTRFC (No.) (%) Proximal RegionTRFC (No.) (%) Distal RegionP Value
    26328 (33.7)15 (18.1).007
    45630 (36.1)6 (7.2)<.001
    64328 (33.7)2 (2.4).001
    83825 (30.1)3 (3.6).022
    103316 (19.3)0 (0)1.0
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American Journal of Neuroradiology: 43 (2)
American Journal of Neuroradiology
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1 Feb 2022
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G.A.J.C. Crombag, M. Aizaz, F.H.B.M. Schreuder, F. Benali, D.H.K. van Dam-Nolen, M.I. Liem, C. Lucci, A.F. van der Steen, M.J.A.P. Daemen, W.H. Mess, A. van der Lugt, P.J. Nederkoorn, J. Hendrikse, P.A.M. Hofman, R.J. van Oostenbrugge, J.E. Wildberger, M.E. Kooi
Proximal Region of Carotid Atherosclerotic Plaque Shows More Intraplaque Hemorrhage: The Plaque at Risk Study
American Journal of Neuroradiology Feb 2022, 43 (2) 265-271; DOI: 10.3174/ajnr.A7384

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Proximal Region of Carotid Atherosclerotic Plaque Shows More Intraplaque Hemorrhage: The Plaque at Risk Study
G.A.J.C. Crombag, M. Aizaz, F.H.B.M. Schreuder, F. Benali, D.H.K. van Dam-Nolen, M.I. Liem, C. Lucci, A.F. van der Steen, M.J.A.P. Daemen, W.H. Mess, A. van der Lugt, P.J. Nederkoorn, J. Hendrikse, P.A.M. Hofman, R.J. van Oostenbrugge, J.E. Wildberger, M.E. Kooi
American Journal of Neuroradiology Feb 2022, 43 (2) 265-271; DOI: 10.3174/ajnr.A7384
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