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The Relationship of Morphological-Hemodynamic Characteristics, Inflammation, and Remodeling of Aneurysm Wall in Unruptured Intracranial Aneurysms

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Abstract

Aneurysm wall remodeling (AWR) is an important pathological characteristic in aneurysm wall, which was characterized by abnormal histological structure and inflammation infiltration. In the present study, the aim is to determine the relationships of morphological-hemodynamic characteristics, inflammation, and AWR in intracranial aneurysms (IAs), as well as the pathological basis of morphological-hemodynamic predictors to achieve IA development. For this end, 113 unruptured IAs were prospectively collected from 110 cases. In addition, patient-specific computational fluid dynamics and geometry were adopted to determine hemodynamic and morphological parameters. Moreover, Hematoxylin-Eosin staining was performed to identify the AWR. By performing immunofluorescence, the inflammatory markers were detected. Masson staining was conducted to characterize the characteristics of atherosclerosis in aneurysm wall. To demonstrate the parameters regarding the AWR, a multivariate logistic analysis was conducted. Besides, correlation analyses were conducted to verify the relationship between morphological-hemodynamic and pathological characteristics. For 113 unruptured IAs, no difference was identified in baseline information. AWR was demonstrated in 92 (81.4%) IAs. To be specific, the aneurysm size (odds ratio (OR), 2.63; confidence interval (CI), 1.04–6.67; P = 0.041), size ratio (SR; OR, 1.95; CI, 1.38–2.76; P < 0.001), normalized wall shear stress average (NWSSA; OR, 0.05; CI, 0.01–0.15; P = 0.007), and relative resident time (RRT; OR, 1.28; CI, 1.07–1.53; P = 0.007) were proved as the factors of AWR. As revealed from the results of immunofluorescence, aneurysm size, SR, NWSSA, and RRT were significantly correlated with the level of inflammation in IA tissues. Furthermore, Masson staining revealed that atherosclerosis area in IA tissues and NWSSA was correlated with RRT. In this study, SR, NWSSA, and RRT were demonstrated as the risk factors of AWR. The mentioned parameters could also reflect the characteristics of inflammation and atherosclerosis in aneurysm wall as well. This study revealed that biomechanical stress and inflammation in aneurysm wall are correlated, which might suggest the pathological evidence of morphological-hemodynamic predictors for IA development.

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Availability of Data and Material

Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

Abbreviations

IA:

Intracranial aneurysm

UIA:

Unruptured intracranial aneurysm

STA:

Superficial temporal artery

CTA:

Computational tomographic angiography

CFD:

Computational fluid dynamics

S:

Aneurysm size

N:

Neck diameter

H:

Perpendicular height

VA:

Vessel angle

AA:

Aneurysm angle

AR:

Aspect ratio

SR:

Size ratio

NSI:

Nonsphericity index

UI:

Undulation index

WSS:

Wall shear stress

WSSA:

Wall shear stress average

WSSM:

Wall shear stress maximum

PA:

Pressure average

WSSA:

Wall shear stress gradient

NWSSA:

Normalized wall shear stress average

NWSSM:

Normalized wall shear stress maximum

NPA:

Normalized pressure average

LSAR:

Low shear area rate

RRT:

Relative resident time

OSI:

Oscillatory shear index

VA:

Vessel angle

AA:

Aneurysm angle

NFKB1:

Nuclear factor-kappa-B 1

IL-2:

Interleukin-2

MMP-2:

Matrix metalloproteinase-2

MMP-9:

Matrix metalloproteinase-9

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Acknowledgements

We thank Jia Liu for providing technical support of computational fluid dynamic analysis.

Funding

This study was supported by the “National Natural Science Foundation of China” (Grant No. 82071296, 81671129, and 81471210) and “Major special projects in the 13th five-year plan” (Grant No. 2016YFC1301800).

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Bei**g Tiantan Hospital, Capital Medical University, No.119 South 4th Ring West Road, Fengtai District, Bei**g, China

    Qingyuan Liu, Junhua Yang, Yi Yang, Maogui Li, Shanwen Chen, Pengjun Jiang, Jun Wu & Shuo Wang

  2. China National Clinical Research Center for Neurological Diseases, Bei**g, China

    Qingyuan Liu, Junhua Yang, Yi Yang, Maogui Li, Shanwen Chen, Pengjun Jiang, Jun Wu & Shuo Wang

  3. Department of Neurointervention, Bei**g Tiantan Hospital, Capital Medical University, No.119 South 4th Ring West Road, Fengtai District, Bei**g, China

    Yisen Zhang

  4. Department of Blood Transfusion, Bei**g Tiantan Hospital, Capital Medical University, No.119 South 4th Ring West Road, Fengtai District, Bei**g, China

    Nuochuan Wang & Yanan Zhang

  5. Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, 85411, Guangdong, China

    Jia Liu

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  1. Qingyuan Liu
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Corresponding authors

Correspondence to Pengjun Jiang or Shuo Wang.

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The work was approved by the Institutional Review Board of Tiantan Hospital (KY2017-076-01).

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(JPG 1715 kb) Supplementary Figure. The pulsatile waveforms at the internal carotid artery of representative cases.

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Liu, Q., Zhang, Y., Yang, J. et al. The Relationship of Morphological-Hemodynamic Characteristics, Inflammation, and Remodeling of Aneurysm Wall in Unruptured Intracranial Aneurysms. Transl. Stroke Res. 13, 88–99 (2022). https://doi.org/10.1007/s12975-021-00917-1

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  • DOI: https://doi.org/10.1007/s12975-021-00917-1

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