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The association between hemodynamics and wall characteristics in human intracranial aneurysms: a review

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Abstract

Hemodynamics plays a key role in the natural history of intracranial aneurysms (IAs). However, studies exploring the association between aneurysmal hemodynamics and the biological and mechanical characteristics of the IA wall in humans are sparse. In this review, we survey the current body of literature, summarize the studies’ methodologies and findings, and assess the degree of consensus among them. We used PubMed to perform a systematic review of studies that explored the association between hemodynamics and human IA wall features using different sources. We identified 28 publications characterizing aneurysmal flow and the IA wall: 4 using resected tissues, 17 using intraoperative images, and 7 using vessel wall magnetic resonance imaging (MRI). Based on correlation to IA tissue, higher flow conditions, such as high wall shear stress (WSS) with complex pattern and elevated pressure, were associated with degenerated walls and collagens with unphysiological orientation and faster synthesis. MRI studies strongly supported that low flow, characterized by low WSS and high blood residence time, was associated with thicker walls and post-contrast enhancement. While significant discrepancies were found among those utilized intraoperative images, they generally supported that thicker walls coexist at regions with prolonged residence time and that thinner regions are mainly exposed to higher pressure with complex WSS patterns. The current body of literature supports a theory of two general hemodynamic-biologic mechanisms for IA development. One, where low flow conditions are associated with thickening and atherosclerotic-like remodeling, and the other where high and impinging flow conditions are related to wall degeneration, thinning, and collagen remodeling.

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Acknowledgements

We would like to thank Dr. Katharina Hackenberg for the constructive discussion and feedback.

Author information

Authors and Affiliations

  1. Canon Stroke and Vascular Research Center, University At Buffalo, State University of New York, 875 Ellicott St., Buffalo, NY, 14203, USA

    Hamidreza Rajabzadeh-Oghaz, Adnan H. Siddiqui, John Kolega & Vincent M. Tutino

  2. Department of Neurosurgery, University At Buffalo, State University of New York, Buffalo, NY, USA

    Hamidreza Rajabzadeh-Oghaz, Adnan H. Siddiqui & Vincent M. Tutino

  3. Department of Radiology, University At Buffalo, State University of New York, Buffalo, NY, USA

    Adnan H. Siddiqui

  4. Department of Mechanical Engineering & Energy Processes, Southern Illinois University, Carbondale, IL, USA

    Arash Asadollahi

  5. Department of Pathology and Anatomical Sciences, University At Buffalo, State University of New York, Buffalo, NY, USA

    John Kolega & Vincent M. Tutino

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  1. Hamidreza Rajabzadeh-Oghaz
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  2. Adnan H. Siddiqui
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  3. Arash Asadollahi
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Contributions

Concept and design: HR-O and VMT; data acquisition: HR-O and AS; data analysis and interpretation: HR-O and VMT; drafting the manuscript: HR-O, VMT, JK, and AHS; critically revising the manuscript: all authors, and final approval of the manuscript: all authors.

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Correspondence to Hamidreza Rajabzadeh-Oghaz.

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Conflict of interest

HR-O: None.

AS: None.

JK: None.

AHS: Research grant: co-investigator of NIH/NINDS 1R01NS091075; financial interest/investor/stock options/ownership: Amnis Therapeutics, Apama Medical, Blink TBI Inc., Buffalo Technology Partners Inc., Cardinal Consultants, Cerebrotech Medical Systems, Inc. Cognition Medical, Endostream Medical Ltd., Imperative Care, International Medical Distribution Partners, Neurovascular Diagnostics Inc., Q’Apel Medical Inc, Rebound Therapeutics Corp., Rist Neurovascular Inc., Serenity Medical Inc., Silk Road Medical, StimMed, Synchron, Three Rivers Medical Inc., Viseon Spine Inc; Consultant/advisory board: Amnis Therapeutics, Boston Scientific, Canon Medical Systems USA Inc., Cerebrotech Medical Systems Inc., Cerenovus, Corindus Inc., Endostream Medical Ltd., Guidepoint Global Consulting, Imperative Care, Integra LifeSciences Corp., Medtronic, MicroVention, Northwest University–DSMB Chair for HEAT Trial, Penumbra, Q’Apel Medical Inc., Rapid Medical, Rebound Therapeutics Corp., Serenity Medical Inc., Silk Road Medical, StimMed, Stryker, Three Rivers Medical, Inc., VasSol, W.L. Gore & Associates; Principal investigator/steering comment of the following trials: Cerenovus NAPA and ARISE II; Medtronic SWIFT PRIME and SWIFT DIRECT; MicroVention FRED & CONFIDENCE; MUSC POSITIVE; and Penumbra 3D Separator, COMPASS, and INVEST.

VMT: Co-founder, Neurovascular Diagnostics, Inc.

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Rajabzadeh-Oghaz, H., Siddiqui, A.H., Asadollahi, A. et al. The association between hemodynamics and wall characteristics in human intracranial aneurysms: a review. Neurosurg Rev 45, 49–61 (2022). https://doi.org/10.1007/s10143-021-01554-w

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