Flow conditions in the intracranial aneurysm lumen are associated with inflammation and degenerative changes of the aneurysm wall

J. Cebral, E. Ollikainen, B. J. Chung, F. Mut, V. Sippola, B. R. Jahromi, R. Tulamo, J. Hernesniemi, M. Niemelä, A. Robertson, J. Frösen

Research output: Contribution to journalArticle

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Abstract

BACKGROUND AND PURPOSE: Saccular intracranial aneurysm is a common disease that may cause devastating intracranial hemorrhage. Hemodynamics, wall remodeling, and wall inflammation have been associated with saccular intracranial aneurysm rupture.Weinvestigated how saccular intracranial aneurysm hemodynamics is associated with wall remodeling and inflammation of the saccular intracranial aneurysm wall. MATERIALS AND METHODS: Tissue samples resected during a saccular intracranial aneurysm operation (11 unruptured, 9 ruptured) were studied with histology and immunohistochemistry. Patient-specific computational models of hemodynamics were created from preoperative CT angiographies. RESULTS: More stable and less complex flows were associated with thick, hyperplastic saccular intracranial aneurysm walls, while slower flows with more diffuse inflow were associated with degenerated and decellularized saccular intracranial aneurysm walls. Wall degeneration (P=.041) and rupture were associated with increased inflammation (CD45+, P=.031). High wall shear stress (P=.018), higher vorticity (P=.046), higher viscous dissipation (P=.046), and high shear rate (P=.046) were associated with increased inflammation. Inflammation was also associated with lack of an intact endothelium (P = .034) and the presence of organized luminal thrombosis (P = .018), though overall organized thrombosis was associated with low minimum wall shear stress (P = .034) and not with the flow conditions associated with inflammation. CONCLUSIONS: Flow conditions in the saccular intracranial aneurysm are associated with wall remodeling. Inflammation, which is associated with degenerative wall remodeling and rupture, is related to high flow activity, including elevated wall shear stress. Endothelial injury may be a mechanism by which flow induces inflammation in the saccular intracranial aneurysm wall. Hemodynamic simulations might prove useful in identifying saccular intracranial aneurysms at risk of developing inflammation, a potential biomarker for rupture.

Original languageEnglish
Pages (from-to)119-126
Number of pages8
JournalAmerican Journal of Neuroradiology
Volume38
Issue number1
DOIs
StatePublished - Jan 2017

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Intracranial Aneurysm
Aneurysm
Inflammation
Rupture
Hemodynamics
Thrombosis
Intracranial Hemorrhages
Endothelium
Histology
Biomarkers
Immunohistochemistry
Wounds and Injuries

Cite this

Cebral, J. ; Ollikainen, E. ; Chung, B. J. ; Mut, F. ; Sippola, V. ; Jahromi, B. R. ; Tulamo, R. ; Hernesniemi, J. ; Niemelä, M. ; Robertson, A. ; Frösen, J. / Flow conditions in the intracranial aneurysm lumen are associated with inflammation and degenerative changes of the aneurysm wall. In: American Journal of Neuroradiology. 2017 ; Vol. 38, No. 1. pp. 119-126.
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title = "Flow conditions in the intracranial aneurysm lumen are associated with inflammation and degenerative changes of the aneurysm wall",
abstract = "BACKGROUND AND PURPOSE: Saccular intracranial aneurysm is a common disease that may cause devastating intracranial hemorrhage. Hemodynamics, wall remodeling, and wall inflammation have been associated with saccular intracranial aneurysm rupture.Weinvestigated how saccular intracranial aneurysm hemodynamics is associated with wall remodeling and inflammation of the saccular intracranial aneurysm wall. MATERIALS AND METHODS: Tissue samples resected during a saccular intracranial aneurysm operation (11 unruptured, 9 ruptured) were studied with histology and immunohistochemistry. Patient-specific computational models of hemodynamics were created from preoperative CT angiographies. RESULTS: More stable and less complex flows were associated with thick, hyperplastic saccular intracranial aneurysm walls, while slower flows with more diffuse inflow were associated with degenerated and decellularized saccular intracranial aneurysm walls. Wall degeneration (P=.041) and rupture were associated with increased inflammation (CD45+, P=.031). High wall shear stress (P=.018), higher vorticity (P=.046), higher viscous dissipation (P=.046), and high shear rate (P=.046) were associated with increased inflammation. Inflammation was also associated with lack of an intact endothelium (P = .034) and the presence of organized luminal thrombosis (P = .018), though overall organized thrombosis was associated with low minimum wall shear stress (P = .034) and not with the flow conditions associated with inflammation. CONCLUSIONS: Flow conditions in the saccular intracranial aneurysm are associated with wall remodeling. Inflammation, which is associated with degenerative wall remodeling and rupture, is related to high flow activity, including elevated wall shear stress. Endothelial injury may be a mechanism by which flow induces inflammation in the saccular intracranial aneurysm wall. Hemodynamic simulations might prove useful in identifying saccular intracranial aneurysms at risk of developing inflammation, a potential biomarker for rupture.",
author = "J. Cebral and E. Ollikainen and Chung, {B. J.} and F. Mut and V. Sippola and Jahromi, {B. R.} and R. Tulamo and J. Hernesniemi and M. Niemel{\"a} and A. Robertson and J. Fr{\"o}sen",
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Cebral, J, Ollikainen, E, Chung, BJ, Mut, F, Sippola, V, Jahromi, BR, Tulamo, R, Hernesniemi, J, Niemelä, M, Robertson, A & Frösen, J 2017, 'Flow conditions in the intracranial aneurysm lumen are associated with inflammation and degenerative changes of the aneurysm wall', American Journal of Neuroradiology, vol. 38, no. 1, pp. 119-126. https://doi.org/10.3174/ajnr.A4951

Flow conditions in the intracranial aneurysm lumen are associated with inflammation and degenerative changes of the aneurysm wall. / Cebral, J.; Ollikainen, E.; Chung, B. J.; Mut, F.; Sippola, V.; Jahromi, B. R.; Tulamo, R.; Hernesniemi, J.; Niemelä, M.; Robertson, A.; Frösen, J.

In: American Journal of Neuroradiology, Vol. 38, No. 1, 01.2017, p. 119-126.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Flow conditions in the intracranial aneurysm lumen are associated with inflammation and degenerative changes of the aneurysm wall

AU - Cebral, J.

AU - Ollikainen, E.

AU - Chung, B. J.

AU - Mut, F.

AU - Sippola, V.

AU - Jahromi, B. R.

AU - Tulamo, R.

AU - Hernesniemi, J.

AU - Niemelä, M.

AU - Robertson, A.

AU - Frösen, J.

PY - 2017/1

Y1 - 2017/1

N2 - BACKGROUND AND PURPOSE: Saccular intracranial aneurysm is a common disease that may cause devastating intracranial hemorrhage. Hemodynamics, wall remodeling, and wall inflammation have been associated with saccular intracranial aneurysm rupture.Weinvestigated how saccular intracranial aneurysm hemodynamics is associated with wall remodeling and inflammation of the saccular intracranial aneurysm wall. MATERIALS AND METHODS: Tissue samples resected during a saccular intracranial aneurysm operation (11 unruptured, 9 ruptured) were studied with histology and immunohistochemistry. Patient-specific computational models of hemodynamics were created from preoperative CT angiographies. RESULTS: More stable and less complex flows were associated with thick, hyperplastic saccular intracranial aneurysm walls, while slower flows with more diffuse inflow were associated with degenerated and decellularized saccular intracranial aneurysm walls. Wall degeneration (P=.041) and rupture were associated with increased inflammation (CD45+, P=.031). High wall shear stress (P=.018), higher vorticity (P=.046), higher viscous dissipation (P=.046), and high shear rate (P=.046) were associated with increased inflammation. Inflammation was also associated with lack of an intact endothelium (P = .034) and the presence of organized luminal thrombosis (P = .018), though overall organized thrombosis was associated with low minimum wall shear stress (P = .034) and not with the flow conditions associated with inflammation. CONCLUSIONS: Flow conditions in the saccular intracranial aneurysm are associated with wall remodeling. Inflammation, which is associated with degenerative wall remodeling and rupture, is related to high flow activity, including elevated wall shear stress. Endothelial injury may be a mechanism by which flow induces inflammation in the saccular intracranial aneurysm wall. Hemodynamic simulations might prove useful in identifying saccular intracranial aneurysms at risk of developing inflammation, a potential biomarker for rupture.

AB - BACKGROUND AND PURPOSE: Saccular intracranial aneurysm is a common disease that may cause devastating intracranial hemorrhage. Hemodynamics, wall remodeling, and wall inflammation have been associated with saccular intracranial aneurysm rupture.Weinvestigated how saccular intracranial aneurysm hemodynamics is associated with wall remodeling and inflammation of the saccular intracranial aneurysm wall. MATERIALS AND METHODS: Tissue samples resected during a saccular intracranial aneurysm operation (11 unruptured, 9 ruptured) were studied with histology and immunohistochemistry. Patient-specific computational models of hemodynamics were created from preoperative CT angiographies. RESULTS: More stable and less complex flows were associated with thick, hyperplastic saccular intracranial aneurysm walls, while slower flows with more diffuse inflow were associated with degenerated and decellularized saccular intracranial aneurysm walls. Wall degeneration (P=.041) and rupture were associated with increased inflammation (CD45+, P=.031). High wall shear stress (P=.018), higher vorticity (P=.046), higher viscous dissipation (P=.046), and high shear rate (P=.046) were associated with increased inflammation. Inflammation was also associated with lack of an intact endothelium (P = .034) and the presence of organized luminal thrombosis (P = .018), though overall organized thrombosis was associated with low minimum wall shear stress (P = .034) and not with the flow conditions associated with inflammation. CONCLUSIONS: Flow conditions in the saccular intracranial aneurysm are associated with wall remodeling. Inflammation, which is associated with degenerative wall remodeling and rupture, is related to high flow activity, including elevated wall shear stress. Endothelial injury may be a mechanism by which flow induces inflammation in the saccular intracranial aneurysm wall. Hemodynamic simulations might prove useful in identifying saccular intracranial aneurysms at risk of developing inflammation, a potential biomarker for rupture.

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U2 - 10.3174/ajnr.A4951

DO - 10.3174/ajnr.A4951

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C2 - 27686488

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EP - 126

JO - American Journal of Neuroradiology

JF - American Journal of Neuroradiology

SN - 0195-6108

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