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High WSS or Low WSS? Complex Interactions of Hemodynamics with Intracranial Aneurysm Initiation, Growth, and Rupture: Toward a Unifying Hypothesis

H. Meng, V.M. Tutino, J. Xiang and A. Siddiqui
American Journal of Neuroradiology July 2014, 35 (7) 1254-1262; DOI: https://doi.org/10.3174/ajnr.A3558
H. Meng
aFrom the Toshiba Stroke and Vascular Research Center (H.M., V.M.T., J.X., A.S.)
bDepartments of Mechanical and Aerospace Engineering (H.M.)
cNeurosurgery (H.M., J.X., A.S.)
dBiomedical Engineering (H.M., V.M.T.), University at Buffalo, State University of New York, Buffalo, New York.
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V.M. Tutino
aFrom the Toshiba Stroke and Vascular Research Center (H.M., V.M.T., J.X., A.S.)
dBiomedical Engineering (H.M., V.M.T.), University at Buffalo, State University of New York, Buffalo, New York.
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J. Xiang
aFrom the Toshiba Stroke and Vascular Research Center (H.M., V.M.T., J.X., A.S.)
cNeurosurgery (H.M., J.X., A.S.)
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A. Siddiqui
aFrom the Toshiba Stroke and Vascular Research Center (H.M., V.M.T., J.X., A.S.)
cNeurosurgery (H.M., J.X., A.S.)
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  • Fig 1.
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    Fig 1.

    Examples of aneurysm growth (A and B) and rupture (C and D) correlated with high wall shear stress and low WSS. A, In a serial study consisting of a baseline and 4 follow-ups, Acevedo-Bolton et al10 found that the maximal growth region (1) of a giant basilar fusiform intracranial aneurysm consistently had the lowest WSS. B, Sugiyama et al13 reported 2 adjacent growing aneurysms, with different hemodynamic characteristics and growing patterns in 1 patient. The proximal growing aneurysm (2) was subjected to local high flow in the growing lobe, while the distal aneurysm (3) was associated with low and oscillatory WSS in the entire aneurysm sac. C, From multivariate statistical analysis of 119 aneurysms, Xiang et al5 found that intracranial aneurysm rupture could be predicted by low WSS and high oscillatory shear index. D, Castro et al11 found, from analysis of 26 aneurysms, that intracranial aneurysm rupture was correlated with high maximum WSS. Images were adapted with permission from the cited references.

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    Fig 2.

    How hemodynamics plays into intracranial aneurysm dynamics. A, Three-way relationship of aneurysmal geometry, flow, and pathobiology. Flow exerts mechanical forces on the vessel wall, eliciting cell-mediated biologic pathways. Sustained changes in flow (thus WSS and pressure) lead to remodeling of the wall, resulting in aneurysm geometry change. In turn, geometry determines the flow, which could drive further biologic processes. B, The balance between growth/repair and degradation/destruction results in aneurysm stability. Aberrant hemodynamics disrupts the balance and amplifies degradation and destruction mechanisms, leading to enlargement and rupture of aneurysm.

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    Fig 3.

    Heterogeneity of saccular aneurysms as a spectrum from type I (A) to type II (D) with various intermediate or combination types in between (B and C). A, A small thin-walled, entirely translucent aneurysm (type I). B, A mostly thin-walled aneurysm with some thicker-walled patches. C, A mostly thick-walled aneurysm with a few thin-walled patches. D, An aneurysm with an entirely thick, atherosclerotic wall (Type II). Images adapted with permission from Kadasi et al 2012.50

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    Fig 4.

    A unified role of high and low WSS in aneurysm initiation, growth, and rupture.

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    Fig 5.

    Two hypothesized, independent, hemodynamic-biologic pathways that drive intracranial aneurysm growth and rupture (A) and the proposed relationship between them and the spectrum of intracranial aneurysm phenotypes (B).

Tables

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  • Vascular responses to aberrant WSS conditions reported in literature

    Pathobiologic Responses to High WSS and Positive WSS GradientaPathobiologic Responses to Low WSS and High OSIb
    EC damage24,45Proinflammatory ECs that are “leaky” and “sticky”21,62
    EC turnover25,72Increased ROS62
    MMP production by mural cells25Increased inflammatory cell infiltration70
    ECM degradation36MMP production by macrophages61
    Medial thinning36SMC proliferation and migration63
    Mural cell apoptosis25Thrombus formation23,63
    • Note:—EC indicates endothelial cell; ROS, reactive oxygen species; MMP, matrix metalloproteinase; OSI, oscillatory shear index; SMC, smooth muscle cell.

    • ↵a From the literature on intracranial aneurysm genesis.

    • ↵b From the literature on atherogenesis.

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American Journal of Neuroradiology: 35 (7)
American Journal of Neuroradiology
Vol. 35, Issue 7
1 Jul 2014
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High WSS or Low WSS? Complex Interactions of Hemodynamics with Intracranial Aneurysm Initiation, Growth, and Rupture: Toward a Unifying Hypothesis
H. Meng, V.M. Tutino, J. Xiang, A. Siddiqui
American Journal of Neuroradiology Jul 2014, 35 (7) 1254-1262; DOI: 10.3174/ajnr.A3558

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High WSS or Low WSS? Complex Interactions of Hemodynamics with Intracranial Aneurysm Initiation, Growth, and Rupture: Toward a Unifying Hypothesis
H. Meng, V.M. Tutino, J. Xiang, A. Siddiqui
American Journal of Neuroradiology Jul 2014, 35 (7) 1254-1262; DOI: 10.3174/ajnr.A3558
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