Micromechanics of elastic lamellae: unravelling the role of structural inhomogeneity in multi-scale arterial mechanics

Abstract

<jats:p>Microstructural deformation of elastic lamellae plays important roles in maintaining arterial tissue homeostasis and regulating vascular smooth muscle cell fate. Our study unravels the underlying microstructural origin that enables elastic lamellar layers to evenly distribute the stresses through the arterial wall caused by intraluminal distending pressure, a fundamental requirement for tissue and cellular function. A new experimental approach was developed to quantify the spatial organization and unfolding of elastic lamellar layers under pressurization in mouse carotid arteries by coupling physiological extension–inflation and multiphoton imaging. Tissue-level circumferential stretch was obtained from analysis of the deformation of a thick-walled cylinder. Our results show that the unfolding and extension of lamellar layers contribute simultaneously to tissue-level deformation. The inner lamellar layers are wavier and unfold more than the outer layers. This waviness gradient compensates the larger tissue circumferential stretch experienced at the inner surface, thus equalizing lamellar layer extension through the arterial wall. Discoveries from this study reveal the importance of structural inhomogeneity in maintaining tissue homeostasis through the arterial wall, and may have profound implications on vascular remodelling in aging and diseases, as well as in tissue engineering of functional blood vessels.</jats:p>

Synchrotron-based visualization and segmentation of elastic lamellae in the mouse carotid artery during quasi-static pressure inflation

“…We observed that lamellar layers unfold in the pressure range between 0 and 30 mm Hg. This is in line with earlier findings of Yu et al [21] and with those of Dobrin, who used radiography to measure the deformation of four elastic lamellae in the dog carotid artery and found complete lamellar unfolding at a pressure between 25 and 55 mm Hg [50]. We also found that lamellar layers stretch (i.e.…”

“…This observation contradicts previous histology-based findings, which suggested that lamellae are only stretched once the intraluminal pressure surpasses the diastolic pressure [51]. It is, however, in line with the observations of Yu et al, who reported that unfolding and extension of lamellar layers contribute simultaneously to tissue-level deformation [21]. Another observation that is consistent with the findings of Yu et al is that the outer interlamellar layer (L23) is slightly thicker than the inner interlamellar layer (L12).…”

“…Since two different samples were used and both samples were embedded in paraffin prior to imaging, there was no direct imaging of how lamellae straighten with pressure [22]. More recently, Yu et al were the first to visualize how distinct lamellar layers in the mouse carotid artery unfold with pressure [21]. Their MPM-based method had limited depth which prevented them from scanning the entire circumference of the vessel.…”

Bioinspired Vascular Grafts

“…The cut ring "opens" to minimize stored strainenergy, as the inner wall is in compression and the outer wall in tension (Humphrey 2002). This residual stress is the result of differences in the waviness of the elastic lamellae between the inner and outer wall (Yu et al 2018a). Direct quantification of residual stress (Λ) is not a simple task.…”

Mechanical Testing of Vascular Grafts

“…To optimize the mechanical function, knowledge in the mechanisms of microstructural deformations and local strains at different loading conditions is important (Disney et al 2018). Fiber sliding, deformation, uncrimping, and alignment are some mechanisms which are investigated in inflation and tensile measurements, combined with optical methods (Yu et al 2018). Measurements on microstructural organization using multiphoton microscopy are also used to establish constitutive models of local mechanical environment within biological tissues and to investigate the relationship between biological responses and mechanical stimuli (Wan et al 2012).…”