Three-Dimensional Collagen Organization of Human Brain Arteries at Different Transmural Pressures

Abstract

Measurements on the directional organization of collagen are necessary for relating the structure and mechanical function of blood vessels. The birefringent optical property of collagen has enabled us to assess the collagen architecture for brain arteries, which are prone to spasm and aneurysm formation. Using the universal stage and polarizing microscope, we measured the three-dimensional organization of the collagen of the main layers of the artery wall, and examined the effect of distending pressure on that organization. Adult arteries obtained from autopsy were fixed at one of three distending pressures, 30, 120 and 200 mm Hg; they were embedded in paraffin and sectioned parallel to the vessel axis at 4 µm thickness. Sections were stained with picrosirius red, a birefringent enhancement stain specific for collagen. Orientation data were obtained from tangential sections from thirteen arteries. We chose to use tangential sections that graze the curving surface of individual layers, to permit measurements that are equally sensitive to fibres in the mechanically meaningful range of directions including longitudinal, helical and circumferential. Each measurement was from a single fibre or group of fibres at a specific location; the mean direction and its variation of alignment within each artery layer were calculated. In some arteries, the adventitia and subendothelium measurements were separated into sublayers, distinguishable by the birefringent optical appearance. Main findings included a substantial component of longitudinal fibres in the adventitia and subendothelium, highly varied in coherence and mean direction, and a thin collagen layer of the adventitia, radially outside the medial muscle cells, that was highly organized circumferentially (circular standard deviation of 9°). At higher pressures, the collagen fabric of all the layers was increasingly coherent and more circumferential in direction.

Microstructural quantification of collagen fiber orientations and its integration in constitutive modeling of the porcine carotid artery

“…The ability to get detailed fiber orientation [6,8,27] and recruitment [7] data makes structural SEFs all the more relevant, such that structural and mechanical model parameters can be separately identified by histological and mechanical experiments, respectively. Specifically, inflation [35,38], planar biaxial [20,24] and uniaxial [11,32] testing are preferable in-vitro mechanical test protocols for vascular tissue.…”

A theoretical model for fibroblast-controlled growth of saccular cerebral aneurysms

“…Most bifurcations of the cerebral vasculature are structurally stable, but a small number develop a weakness that causes the wall to expand outwardly in the region near the flow divider of the branching artery (Austin et al, 1993;MacDonald et al, 2000;Rowe et al, 2003). Some measurements of the macroscopic mechanical properties of cerebral arteries and aneurysms exist (Coulson et al, 2004;Monson et al, 2003Monson et al, , 2005Scott et al, 1972;Steiger, 1990;Tóth et al, 1998Tóth et al, , 2005 and the structural organisation of these tissues is fairly well documented (Canham et al, 1991b(Canham et al, ,a, 1992(Canham et al, , 1996(Canham et al, , 1999Finlay et al, 1991Finlay et al, , 1995Finlay et al, , 1998Hassler, 1972;MacDonald et al, 2000;Rowe et al, 2003;Smith et al, 1981;Whittaker et al, 1988). In the aneurysmal wall, the tunica media and the internal elastic lamina have often disappeared or are severely fragmented (Abruzzo et al, 1998;Sakaki et al, 1997;Stehbens, 1963;Suzuki and Ohara, 1978;Tóth et al, 1998).…”

“…Thus, the wall of saccular cerebral aneurysms can roughly be described as a development of the adventitia of the original healthy artery (Abruzzo et al, 1998;Scanarini et al, 1978;Schievink, 1997). In the media of a healthy cerebral artery, the smooth muscle and collagen components are almost perfectly aligned in the circumferential direction of the artery (Finlay et al, 1995;Walmsley et al, 1983), whereas the collagen of the adventitia (which dominates the mechanical behaviour of this layer) shows a dispersion from the circumferential to the longitudinal orientation (Finlay et al, 1995;Smith et al, 1981).…”

Constitutive modelling of arteries considering fibre recruitment and three-dimensional fibre distribution

“…Measurements of the fibre orientation [16,18] suggest two fibre families in arterial tissue with a non-symmetric distribution around a mean fibre direction. This mean fibre direction is identified by a which is the angle between the circumferential direction of the arterial wall and the direction with the highest density of fibres, the 'mean fibre angle' (figure 1c).…”