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Research ArticleAdult Brain

Quantification of Oscillatory Shear Stress from Reciprocating CSF Motion on 4D Flow Imaging

S. Yamada, H. Ito, M. Ishikawa, K. Yamamoto, M. Yamaguchi, M. Oshima and K. Nozaki
American Journal of Neuroradiology March 2021, 42 (3) 479-486; DOI: https://doi.org/10.3174/ajnr.A6941
S. Yamada
aFrom the Department of Neurosurgery (S.Y., K.N.), Shiga University of Medical Science, Shiga, Japan
bDepartment of Neurosurgery and Normal Pressure Hydrocephalus Center (S.Y., K.Y., M.Y.), Rakuwakai Otowa Hospital, Kyoto, Japan
cInterfaculty Initiative in Information Studies/Institute of Industrial Science (S.Y., M.O.), The University of Tokyo, Tokyo, Japan
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H. Ito
dMedical System Research and Development Center (H.I.), Fujifilm Corporation, Tokyo, Japan
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M. Ishikawa
eRakuwa Villa Ilios (M.I.), Kyoto, Japan
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K. Yamamoto
bDepartment of Neurosurgery and Normal Pressure Hydrocephalus Center (S.Y., K.Y., M.Y.), Rakuwakai Otowa Hospital, Kyoto, Japan
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M. Yamaguchi
bDepartment of Neurosurgery and Normal Pressure Hydrocephalus Center (S.Y., K.Y., M.Y.), Rakuwakai Otowa Hospital, Kyoto, Japan
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M. Oshima
cInterfaculty Initiative in Information Studies/Institute of Industrial Science (S.Y., M.O.), The University of Tokyo, Tokyo, Japan
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K. Nozaki
aFrom the Department of Neurosurgery (S.Y., K.N.), Shiga University of Medical Science, Shiga, Japan
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  • FIG 1.
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    FIG 1.

    Schema explaining OSS: θ(n) is the angle between Embedded Image and Embedded Image in the nth phase Embedded Image(n) Embedded Image Where Embedded Image indicates a vector of TAWSS, and Embedded Image indicates a vector of WSS.

  • FIG 2.
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    FIG 2.

    Oscillation of WSS due to bidirectional CSF flow through the cerebral aqueduct. The numbers 1, 2, and 3 demonstrate temporal changes of the reciprocating CSF motion during 1 cardiac cycle in a 77-year-old man diagnosed with iNPH. The colored path lines (lower figures) show the flow as a moving trajectory of the virtual particle through the middle part of the cerebral aqueduct in 1 heartbeat. The color and length of 3D streamlines (upper figures) indicate the flow velocity as pink for fast and blue for slow. The sampling interval of streamlines and path lines was set at 0.2 mm after the trilinear interpolation. The arrows indicate the WSS vector produced by the flow parallel to the wall surface. The size and direction of the arrows indicate the magnitude and direction of the WSS vector. Temporal changes of the WSS vector at the dorsal region (yellow arrows) were larger than those at the ventral region (white arrows).

  • FIG 3.
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    FIG 3.

    Distributions and fluctuations of shear stress parameters per heartbeat in iNPH. The colored surfaces in the ventricles show the distribution of WSS magnitude (A) and OSI (B) in the same patient with iNPH, as shown in Fig 2. Red indicates high and blue indicates low. Line-graphs C and D show chronologic changes of WSS magnitude and OSS at the dorsal region of the foramen magnum (ROI 2, yellow) and dorsal (ROI 3, red) and ventral (ROI 4, blue) regions of the cerebral aqueduct in 1 cardiac cycle. Considering the shear stress direction, these changes were completely different.

  • FIG 4.
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    FIG 4.

    Boxplots for the amplitude of OSS and TAWSS at the dorsal and ventral regions of the cerebral aqueduct among 3 groups. A, Distribution of the OSS amplitude at the dorsal region of the cerebral aqueduct. B, Distribution of the TAWSS at the dorsal region of the cerebral aqueduct. C, Distribution of the OSS amplitude at the ventral region of the cerebral aqueduct. D, Distribution of the TAWSS at the ventral region of the cerebral aqueduct.

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    Table 1:

    Clinical and morphologic characteristics of the study populationa

    iNPH OnlyiNPH with ADControlP Value
    Total number41239
    Male/female28:1313:104:5.332
    Age (yr)78.2 [SD, 6.62]79.8 [SD, 5.83]75.7 [SD, 5.70].207
    Anteroposterior diameter (mm)
     Foramen of Magendie5.72 [SD, 1.77]5.88 [SD, 2.04]2.02 [SD, 0.44]<.001
     Lower end of cerebral aqueduct4.44 [SD, 0.87]4.25 [SD, 1.41]2.23 [SD, 0.70]<.001
     Upper end of cerebral aqueduct3.65 [SD, 0.66]3.45 [SD, 0.73]2.30 [SD, 0.54]<.001
     Midbrain8.56 [SD, 0.88]8.43 [SD, 0.92]9.32 [SD, 1.57].230
    Stroke volume (μL/heartbeat)
     Foramen of Magendie32.9 [SD, 22.6]37.4 [SD, 37.6]21.1 [SD, 11.7].448
     Lower end of cerebral aqueduct37.6 [SD, 28.9]39.6 [SD, 43.7]17.8 [SD, 13.0].083
     Upper end of cerebral aqueduct49.0 [SD, 33.3]52.6 [SD, 32.5]18.9 [SD, 10.5].002
     Foramina of Monro96.5 [SD, 41.0]97.8 [SD, 39.1]62.8 [SD, 44.6].042
    • a Data are means. P value is from the Kruskal-Wallis rank sum test.

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    Table 2:

    Mean value [SD] of parameters at the cerebral aqueduct in the study populationa

    All (n = 73)iNPH Only (n = 41)iNPH with AD (n = 23)Control (n = 9)P1P2P3
    Dorsal region of the cerebral aqueduct
     OSS amplitude52.5 [SD, 33.9]59.7 [SD, 34.1]52.9 [SD, 32.2]19.8 [SD, 13.3].483<.001.004
     Maximum OSS35.9 [SD, 16.0]38.7 [SD, 15.5]37.3 [SD, 16.1]19.7 [SD, 6.3].566<.001.002
     Minimum OSS–16.7 [SD, 19.8]–21.0 [SD, 20.2]–15.6 [SD, 18.9]–0.1 [SD, 9.6].277.001.043
     TAWSS18.2 [SD, 8.9]19.7 [SD, 8.7]18.8 [SD, 9.3]9.9 [SD, 2.2].678<.001.008
     OSI0.21 [SD, 0.13]0.24 [SD, 0.12]0.19 [SD, 0.14]0.16 [SD, 0.11].234.077.614
    Ventral region of the cerebral aqueduct
     OSS amplitude27.2 [SD, 28.4]36.0 [SD, 32.2]18.1 [SD, 19.8]11.9 [SD, 11.1].022.020.363
     Maximum OSS23.6 [SD, 15.9]28.8 [SD, 17.9]18.2 [SD, 10.9]14.2 [SD, 6.4].017.011.246
     Minimum OSS–3.6 [SD, 13.9]–7.1 [SD, 15.9]0.14 [SD, 10.1]2.3 [SD, 7.5].080.091.592
     TAWSS12.2 [SD, 7.1]14.3 [SD, 8.1]10.1 [SD, 4.9]8.1 [SD, 2.7].038.020.458
     OSI0.13 [SD, 0.15]0.15 [SD, 0.15]0.10 [SD, 0.14]0.11 [SD, 0.15].114.355.910
    • ↵a P1 indicates probability value of iNPH only versus iNPH with AD by the Wilcoxon rank sum test; P2, probability value of iNPH only versus controls by the Wilcoxon rank sum test; and P3, probability value of iNPH with AD versus controls by the Wilcoxon rank sum test.

    • View popup
    Table 3:

    Relationships with anterior-posterior diameter by the Pearson correlation coefficient (95% confidence intervals)

    Foramen of MagendieLower End of Cerebral AqueductUpper End of Cerebral AqueductMidbrain
    Dorsal region of the cerebral aqueduct
     OSS amplitude0.55 (0.36–0.69)0.47 (0.26–0.63)0.28 (0.05–0.48)NS
     Maximum OSS0.53 (0.34–0.68)0.41 (0.20–0.59)NSNS
     Minimum OSS–0.51 (–0.66 to –0.31)–0.46 (–0.63 to –0.26)–0.32 (–0.51 to –0.10)NS
     TAWSS0.56 (0.37–0.70)0.40 (0.18–0.58)NSNS
     OSINSNSNSNS
    Ventral region of the cerebral aqueduct
     OSS amplitudeNS0.27 (0.04–0.47)NSNS
     Maximum OSSNS0.31 (0.08–0.50)NSNS
     Minimum OSSNSNSNSNS
     TAWSS0.26 (0.04–0.47)0.33 (0.10–0.52)NSNS
     OSINSNSNSNS
    • Note:—NS indicates not significant (P ≥ .05) by the Pearson correlation analysis.

    • View popup
    Table 4:

    Relationships with stroke volume by the Pearson correlation coefficient (95% confidence intervals)

    Foramen of MagendieLower End of Cerebral AqueductUpper End of Cerebral AqueductForamina of Monro
    Dorsal region of the cerebral aqueduct
     OSS amplitude0.48 (0.28–0.64)0.53 (0.34–0.68)0.63 (0.47–0.76)NS
     Maximum OSS0.50 (0.31–0.66)0.56 (0.37–0.70)0.66 (0.50–0.77)NS
     Minimum OSS–0.41 (–0.59 to –0.20)–0.46 (–0.63 to –0.26)–0.55 (–0.70 to –0.37)NS
     TAWSS0.43 (0.22–0.60)0.53 (0.34–0.68)0.73 (0.60–0.82)NS
     OSINSNSNSNS
    Ventral region of the cerebral aqueduct
     OSS amplitudeNS0.30 (0.07–0.50)0.25 (0.02–0.46)NS
     Maximum OSSNS0.32 (0.10–0.52)0.29 (0.07–0.49)NS
     Minimum OSSNS–0.24 (–0.45 to –0.01)NSNS
     TAWSSNS0.37 (0.15–0.55)0.34 (0.12–0.53)NS
     OSINSNSNSNS
    • Note:—NS indicates not significant (P ≥ .05) by the Pearson correlation analysis.

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American Journal of Neuroradiology: 42 (3)
American Journal of Neuroradiology
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S. Yamada, H. Ito, M. Ishikawa, K. Yamamoto, M. Yamaguchi, M. Oshima, K. Nozaki
Quantification of Oscillatory Shear Stress from Reciprocating CSF Motion on 4D Flow Imaging
American Journal of Neuroradiology Mar 2021, 42 (3) 479-486; DOI: 10.3174/ajnr.A6941

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Quantification of Oscillatory Shear Stress from Reciprocating CSF Motion on 4D Flow Imaging
S. Yamada, H. Ito, M. Ishikawa, K. Yamamoto, M. Yamaguchi, M. Oshima, K. Nozaki
American Journal of Neuroradiology Mar 2021, 42 (3) 479-486; DOI: 10.3174/ajnr.A6941
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