Differential structural adaptation to haemodynamics along single rat cremaster arterioles

Abstract

We tested the hypothesis that under physiological conditions, arterioles match their diameter to the level of shear stress. Haemodynamic and anatomical data were obtained in segments of the first-order arteriole of the rat cremaster muscle. Along this segment of ~10 mm in length, local blood pressure decreased from 68 +/- 4 mmHg upstream to 54 +/- 3 mmHg downstream (n = 5). Pulse pressure decreased from 8.2 +/- 1.3 mmHg upstream to 4.1 +/- 0.6 mmHg downstream. At the same locations, an increase in arteriolar diameter was measured in vivo, from 179 +/- 4 microm upstream to 203 +/- 4 microm downstream (n = 10). In vitro pressure-diameter relations of maximally dilated vessels showed that the passive diameter was larger in downstream than upstream segments over a 15-125 mmHg pressure range (n = 18). The wall stress was similar for the upstream vs. downstream location: 266 +/- 16 vs. 260 +/- 14 mN mm-2. However, shear stress decreased from 30 +/- 5 to 21 +/- 5 dyn cm-2 (3.0 +/- 0.5 to 2.1 +/- 0.5 N m-2; n = 4) along the artery. In conclusion, these results demonstrate that shear stress is not the only factor in determining vascular calibre. We suggest that arteriolar calibre may rather depend on an interplay between shear stress and the local pressure profile.

Figure 1. Overview of the preparation for in situ measurements

The cremaster muscle was exposed through a dorsal incision of the skin. The first-order arteriole (left) has one small side branch in this example (arrow). Locations of measurement for combined intravascular pressure and lumen diameter or combined red blood cell velocity and diameter are indicated. Note that the diameter of the arteriole increases gradually along the vessel.

Figure 2. Examples of intravascular pressure recordings using the servo-null method

Tracings are plotted along the same time scale but were recorded non-simultaneouly. Note the decrease in both mean pressure and amplitude of pressure oscillation from upstream to downstream.

Figure 3. Overview of data obtained in vivo

A, intravascular pressure measurements of individual experiments. Upstream and downstream measurements were made in five rats. A significant decrease in pressure was found along the vessel (P = 0.0007). B, diameter measurements of individual experiments. Upstream and downstream lumen diameter was measured in situ in 10 rats in the closed and open cremaster preparation as indicated. A significant increase in diameter between the upstream and downstream location was found (P < 0.001). C, diameter measurements along the length of an additional four individual segments in situ. D, calculated shear stress of individual experiments. Mean shear stress decreased significantly along the vessel (P < 0.05).

Figure 4. Pressure-diameter relations of arteries in vitro

A, pressure-diameter relation of maximally dilated arterioles from cremaster muscle tested in vitro (n = 18). Upstream segments were significantly smaller than their paired downstream counterparts at all pressures tested (P < 0.001). B, pressure-diameter relation of maximally dilated small epigastric arteries in vitro (n = 6). A significant increase in diameter was found along the artery at all pressure levels, with exception of the lowest pressure level.

Figure 5. Example of cross-sections of the cremaster muscle at P = 0 mmHg, stained with elastin-van Gieson

The first-order arteriole at the upstream location (left) and downstream location (right). At the upstream location, the arteriole has a smaller diameter and the vessel wall is more folded.