Local characterization of collagen architecture and mechanical failure properties of fibrous plaque tissue of atherosclerotic human carotid arteries

Local characterization of collagen architecture and mechanical failure properties of fibrous plaque tissue of atherosclerotic human carotid arteries

Torun, Su Guvenir (Erasmus MC)
Munoz, Pablo de Miguel (Student TU Delft; Erasmus MC)
Crielaard, Hanneke (Erasmus MC)
Verhagen, Hence J.M. (Erasmus MC)
Kremers, Gert Jan (Erasmus MC)
van der Steen, A.F.W. (TU Delft ImPhys/Medical Imaging; TU Delft ImPhys/Verweij group; Erasmus MC)
Akyildiz, A.C. (TU Delft Medical Instruments & Bio-Inspired Technology; Erasmus MC)

2023

Atherosclerotic plaque rupture in carotid arteries is a major cause of cerebrovascular events. Plaque rupture is the mechanical failure of the heterogeneous fibrous plaque tissue. Local characterization of the tissue's failure properties and the collagen architecture are of great importance to have insights in plaque rupture for clinical event prevention. Previous studies were limited to average rupture properties and global structural characterization, and did not provide the necessary local information. In this study, we assessed the local collagen architecture and failure properties of fibrous plaque tissue, by analyzing 30 tissue strips from 18 carotid plaques. Our study framework entailed second harmonic generation imaging for local collagen orientation and dispersion, and uniaxial tensile testing and digital image correlation for local tissue mechanics. The results showed that 87% of the imaged locations had collagen orientation close to the circumferential direction (0°) of the artery, and substantial dispersion locally. All regions combined, median [Q1:Q3] of the predominant angle measurements was -2° [-16°:16°]. The stretch ratio measurements clearly demonstrated a nonuniform stretch ratio distribution in the tissue under uniaxial loading. The rupture initiation regions had significantly higher stretch ratios (1.26 [1.15-1.40]) than the tissue average stretch ratio (1.11 [1.10-1.16]). No significant difference in collagen direction and dispersion was identified between the rupture regions and the rest of the tissue. The presented study forms an initial step towards gaining better insights into the characterization of local structural and mechanical fingerprints of fibrous plaque tissue in order to aid improved assessment of plaque rupture risk. Statement of significance: Plaque rupture risk assessment, critical to prevent cardiovascular events, requires knowledge on local failure properties and structure of collagenous plaque tissue. Our current knowledge is unfortunately limited to tissue's overall ultimate failure properties with scarce information on collagen architecture. In this study, local failure properties and collagen architecture of fibrous plaque tissue were obtained. We found predominant circumferential alignment of collagen fibers with substantial local dispersion. The tissue showed nonuniform stretch distribution under uniaxial tensile loading, with high stretches at rupture spots. This study highlights the significance of local mechanical and structural assessment for better insights into plaque rupture and the potential use of local stretches as risk marker for plaque rupture for patient-specific clinical applications.

Atherosclerosis
Digital image correlation
Mechanical testing
Plaque rupture
Second harmonic generation

http://resolver.tudelft.nl/uuid:00c64bf9-b9b7-43b5-a82f-32ded4ad5dc3

https://doi.org/10.1016/j.actbio.2023.04.022

1742-7061

Acta Biomaterialia, 164, 293-302

Institutional Repository

journal article

© 2023 Su Guvenir Torun, Pablo de Miguel Munoz, Hanneke Crielaard, Hence J.M. Verhagen, Gert Jan Kremers, A.F.W. van der Steen, A.C. Akyildiz