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Research ArticleAdult Brain
Open Access

Perivascular Spaces in Old Age: Assessment, Distribution, and Correlation with White Matter Hyperintensities

A. Laveskog, R. Wang, L. Bronge, L.-O. Wahlund and C. Qiu
American Journal of Neuroradiology January 2018, 39 (1) 70-76; DOI: https://doi.org/10.3174/ajnr.A5455
A. Laveskog
aFrom the Division of Radiology (A.L.), Department of Clinical Science, Intervention and Technology
dDepartment of Neuroradiology (A.L.), Karolinska University Hospital, Stockholm, Sweden
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R. Wang
bAging Research Center (R.W., C.Q.), Department of Neurobiology, Care Sciences and Society
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L. Bronge
cDepartment of Clinical Neuroscience (L.B.), Karolinska Institutet, Stockholm, Sweden
eAleris Diagnostics (L.B.), Sabbatsberg, Stockholm, Sweden
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L.-O. Wahlund
fDivision of Clinical Geriatrics (L.-O.W.), Department of Neurobiology, Care Sciences and Society, Karolinska University Hospital at Huddinge, Stockholm, Sweden.
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C. Qiu
bAging Research Center (R.W., C.Q.), Department of Neurobiology, Care Sciences and Society
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    Fig 1.

    Sample images of grades 0–3 for the number of perivascular spaces bilaterally in the basal ganglia medial to the external capsule. The images indicate grade 0 (A), grade 1 (B), grade 2 (C), and grade 3 (D) in the basal ganglia. Note that the perivascular spaces contributing to the score might be in another level and thus not visible in the sample images.

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    Fig 2.

    Sample images of PVS with different grades. A and B, Grade 3 in number and grade 1 in size of PVS in the subinsular, basal ganglia, frontal, and parietal regions. There are >10 PVS in each region, but none of the PVS are wider than 2 mm. In the basal ganglia, PVS are seen as dots (oval) because the image is acquired cross-sectional to the vessels (A, axial T1), while PVS are linear in the frontal and parietal lobe (arrows), where the vessels are in a plane with the image (B, axial T2). C, Grade 3 in number and grade 1 in size in the left hippocampus (oval, axial T2). PVS in the hippocampus are really hippocampal sulcus remnants, which can be clearly seen in D (arrow, coronal T1).

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    Fig 3.

    Age-specific distribution of global scores for the number, size, and a combination of both number and size of PVS. Note that there are 3 subjects with missing values in the global PVS score for size.

Tables

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    Table 1:

    Demographic and clinical characteristics of study participants by sex

    CharacteristicsTotal SampleMenWomenP Valuea
    No. of subjects530218312
    Age (yr) (No.) (%)
        60141 (26.6)66 (30.3)75 (24.0)
        66123 (23.2)51 (23.4)72 (23.1)
        7284 (15.8)30 (13.8)54 (17.3)
        7873 (13.8)29 (13.3)44 (14.1)
        8149 (9.2)18 (8.3)31 (9.9)
        8426 (4.9)9 (4.1)17 (5.4)
        8718 (3.4)9 (4.1)9 (2.9)
        90 or older16 (3.0)6 (2.8)10 (3.2).72
    Age (yr), mean (SD)70.7 (9.1)70.1 (9.2)71.1 (9.0).20
    Education (No.) (%)
        Primary school67 (12.6)26 (11.9)41 (13.1)
        Middle school246 (46.4)78 (35.8)168 (53.8)
        University217 (40.9)114 (52.3)103 (33.0)<.01
    Hypertension (No.) (%)383 (72.3)165 (75.7)218 (69.9).14
    Diabetes (No.) (%)41 (7.7)25 (11.5)16 (5.1)<.01
    High cholesterol (No.) (%)295 (56.4)118 (55.7)177 (56.9).78
    Obesity (No.) (%)72 (13.6)30 (13.8)42 (13.5).93
    Atrial fibrillation (No.) (%)11 (2.1)7 (3.2)4 (1.3).13
    Coronary heart disease (No.) (%)53 (10.0)30 (13.8)23 (7.4).02
    Heart failure (No.) (%)12 (2.3)5 (2.3)7 (2.2).97
    PVH (median) (IQR)8 (6–9)8 (6–10)8 (6–9).56
    WMH (median) (IQR)16 (5–29)16 (4–26)16 (6–30).56
    • Note:—IQR indicates interquartile range.

    • ↵a P value was for the test of sex differences.

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    Table 2:

    Distribution of regional perivascular spaces by number and sizea

    Hemispheres and RegionsNo. of Perivascular SpacesSize (mm in Diameter) of Perivascular Spacesb
    None1–56–10>10None1–23–4>4
    Left
        Frontal32 (6.0)70 (13.2)107 (20.2)321 (60.6)32 (6.0)473 (89.3)25 (4.7)0
        Parieto-occipital25 (4.7)68 (12.8)116 (21.9)321 (60.6)25 (4.7)486 (91.7)16 (3.0)3 (0.6)
        Basal ganglia085 (16.0)240 (45.3)205 (38.7)0443 (83.6)80 (15.1)7 (1.3)
        Subinsular128 (24.2)277 (52.3)107 (20.2)18 (3.4)128 (24.2)370 (69.9)30 (5.7)1 (0.2)
        Hippocampus156 (29.4)328 (61.9)46 (8.7)0156 (29.4)348 (65.7)26 (4.9)0
        Mesencephalon255 (48.1)274 (51.9)00254 (47.9)273 (51.5)3 (0.6)0
        Cerebellum456 (86.0)74 (14.0)00456 (86.0)74 (14.0)00
    Right
        Frontal28 (5.3)64 (12.1)94 (17.7)344 (64.9)28 (5.3)474 (89.4)27 (5.1)1 (0.2)
        Parieto-occipital29 (5.5)79 (14.9)106 (20.0)316 (59.6)29 (5.5)487 (91.9)14 (2.6)0
        Basal ganglia1 (0.2)103 (19.4)231 (43.6)195 (36.8)1 (0.2)452 (85.3)63 (11.9)14 (2.6)
        Subinsular131 (24.7)280 (52.8)103 (19.4)16 (3.0)131 (24.7)369 (69.6)29 (5.5)1 (0.2)
        Hippocampus210 (39.6)284 (53.6)35 (6.6)1 (0.2)209 (39.5)292 (55.2)26 (4.9)2 (0.4)
        Mesencephalon263 (49.6)265 (50.0)2 (0.4)0262 (49.5)263 (49.7)4 (0.8)0
        Cerebellum462 (87.2)68 (12.8)00463 (87.4)67 (12.6)00
    • ↵a Data are No. (%).

    • ↵b There were missing values of perivascular space size in 1 subject in the mesencephalon (right hemisphere), 1 in the hippocampus (right hemisphere), and 1 in the basal ganglia (left hemisphere).

    • View popup
    Table 3:

    Partial correlation coefficients between PVS and WMH scoresa

    Global and Regional PVS ScoresWMH Scores
    GlobalLobar White Matter AreasbDeep White Matter AreasbPeriventricular Regionsb
    PVS score, total
        Global region0.204c0.182c0.171c0.066
        Frontal region0.0400.0480.0110.007
        Parieto-occipital region0.0280.0170.0280.031
        Basal ganglia0.318c0.256c0.292c0.160c
        Subinsular region0.228c0.206c0.173c0.101d
        Hippocampus0.127c0.137c0.0720.021
        Mesencephalon0.0440.0440.073−0.077
        Cerebellum0.0710.0340.110d0.039
    PVS score (No.)
        Global region0.206c0.177c0.183c0.074
        Frontal region0.0340.0390.0150.001
        Parieto-occipital region0.002−0.0130.0180.022
        Basal ganglia0.355c0.295c0.303c0.194c
        Subinsular region0.263c0.223c0.233c0.111d
        Hippocampus0.101d0.117c0.051−0.004
        Mesencephalon0.0410.0440.067−0.081
        Cerebellum0.0710.0340.11d0.037
    PVS score (size)
        Global region0.184c0.177c0.140c0.042
        Frontal region0.0460.061−0.0040.023
        Parieto-occipital region0.109d0.113d0.0520.053
        Basal ganglia0.0700.0420.107d0.008
        Subinsular region0.143d0.152d0.0590.073
        Hippocampus0.151c0.154c0.092d0.043
        Mesencephalon0.0020.0120.029−0.096d
        Cerebellum0.0710.0330.1110.041
    • ↵a The correlation coefficients were adjusted for age, sex, and education.

    • ↵b Lobar white matter areas include the frontal, parieto-occipital, and temporal lobes in both hemispheres; deep white matter areas include the basal ganglia, capsular, thalami, pons, and mesencephalon; and periventricular areas include the frontal, lateral, and occipital periventricular areas.

    • ↵c P < .01.

    • ↵d P < .05.

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A. Laveskog, R. Wang, L. Bronge, L.-O. Wahlund, C. Qiu
Perivascular Spaces in Old Age: Assessment, Distribution, and Correlation with White Matter Hyperintensities
American Journal of Neuroradiology Jan 2018, 39 (1) 70-76; DOI: 10.3174/ajnr.A5455

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Perivascular Spaces in Old Age: Assessment, Distribution, and Correlation with White Matter Hyperintensities
A. Laveskog, R. Wang, L. Bronge, L.-O. Wahlund, C. Qiu
American Journal of Neuroradiology Jan 2018, 39 (1) 70-76; DOI: 10.3174/ajnr.A5455
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