Elsevier

Journal of Biomechanics

Volume 112, 9 November 2020, 110065
Journal of Biomechanics

Time-course of axial residual strain remodeling and layer-specific thickening during aging along the human aorta

https://doi.org/10.1016/j.jbiomech.2020.110065Get rights and content

Abstract

Detailed estimation of axial residual strains in the human aorta is necessary when performing biomechanical analyses of physiologic functions and pathologic conditions. We recently published such data for autopsied aortas and the present aim was to measure axial residual stretches at different wall depths, along with layer thicknesses on images borrowed from that work. Residual stretches at the external surface and medial-adventitial interface increased along the aorta’s ascending course, decreased along its descending course, and increased from the diaphragm toward the iliac arteries. Residual stretches at the intimal-medial interface and internal surface decreased down the distal one-third of the aorta. A continuous decrease in medial thickness was witnessed along the vessel, whereas intimal and adventitial thickness remained fairly stable. At some axial locations, smaller were the axial residual stretches of the outer than those of the other quadrants, with minor differences in layer-specific thicknesses among quadrants. Adventitial thickness did not vary with age, while the intima and media thickened considerably with different time-courses. The observed intimal thickening solely between young (≤40 yr) and middle-aged subjects (40–60 yr) is consistent with the increased circumferential residual stretches previously established by our group between those subject groups and the minimal further increase in old subjects (≥60 yr). The observed medial thickening between middle-aged and old subjects was accompanied by decreased axial residual stretches that were not seen between young and middle-aged subjects. These observations suggest distinct roles for the intima and media in determining circumferential and axial residual stretches that merit further attention.

Introduction

The aorta is the conduit through which blood ejected from the heart is delivered to the organs and tissues of the body. Other than its conduit function, the biomechanical properties serve a buffering function. The aorta is distended during systole, storing a portion of the stroke volume, and recoils during diastole, allowing a continuous blood flow to the periphery (Boudoulas and Wooley, 1996, Nichols et al., 2011). Due to its incessant exposure to high pulsatile pressure and shear stress, it is susceptible to injury caused by biomechanical trauma, e.g., dissection and rupture, and to aneurysm formation governed by biomechanical principles (Creager and Loscalzo, 2018). In-depth knowledge of the biomechanical properties of the aortic wall and how these vary lengthwise and perimeter-wise is key to understanding the functions of the aorta, and its pathologic/catastrophic conditions (Humphrey, 2002).

Despite recent advances, our knowledge of the zero-stress state of the human aorta and the database of its geometry are still limited, precluding sophisticated biomechanical analysis of these aortic conditions. Circumferential residual strains in animal aortas were first documented by Chuong and Fung (1986), and Vaishnav and Vossoughi (1987); thereafter, Vossoughi (1992) documented the existence of axial residual strains. Circumferential residual strains regulate the local biomechanical environment of cells by homogenizing the in vivo transmural stress gradients and the zero-stress state constitutes the reference configuration for developing material models; see the seminal review articles by Fung (1991), and Rachev and Greenwald (2003). Saini et al. (1995) published initial data on the circumferential zero-stress state of human aorta at six locations and, in the absence of more complete data, our group evaluated both circumferential and axial residual strains all over the vessel (Sokolis et al., 2017, Sokolis et al., 2020).

In the present communication, we studied the transmural distribution of axial residual strains by measuring them at the layer interfaces on images borrowed from (Sokolis et al., 2020). The time-course of layer thickening with aging was examined as a function of axial and circumferential location, for which information is currently unavailable. Our data propose distinct intimal and medial roles in determining residual stretches in the two principal directions.

Section snippets

Study population

The material used was the same as that in our companion publication (Sokolis et al., 2020). In particular, full-length aortas were removed within 24 h of death from twenty-three autopsy subjects, thirteen of whom were males and ten females; age range: 23–87 yr, mean ± standard error (SE): 50 ± 7 yr. Inclusion criteria were age > 18 yr and absence of aortic aneurysm/dissection or connective tissue disorders. The aortas were stored in 0.9% saline at 4 °C and studied within 12 h of removal.

Axial zero-stress state determination

Results and discussion

The outermost residual stretches for pooled data from all subjects and quadrants varied alike with axial location, as did the innermost residual stretches (Fig. 2). The former rose along the ascending aorta and ascending course of the arch, declined along its downward course remaining constant until the diaphragm, and rose again to their greatest values toward the iliac arteries. In contrast, the latter were relatively unchanged down the central two-thirds of the aorta, exhibiting a decreasing

Acknowledgements

The author wishes to thank Mr. A. Bompas for his valuable assistance in initiating this study.

Declaration of Competing Interest

The author declares no competing interests.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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      Unlike outer-layer thickness, intact-wall and inner-layer thicknesses varied less along the aorta of middle-aged and old subjects. These findings agree with our previous intact-wall (Sokolis et al., 2017; 2020) and layer-specific thickness measurements (Sokolis, 2020) [refer also to (Concannon et al., 2020)], noting that the inner layers in the present tests included the intima with most of the media and the outer layers included the leftover media with the adventitia. The dissection plane was initiated adjacent to the external elastic lamina, based on our previous study (Manopoulos et al., 2018) on the tensile strength of the dissected ascending aorta which confirmed histologically the clinical observation that dissection propagates within the outer third of the media (Roberts, 1981).

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