Effects of temperature on the wall strength and compliance of frog mesenteric microvessels

Autor: C. C. Michel, C. R. Neal
Rok vydání: 2000
Předmět:
Zdroj: The Journal of Physiology. 526:613-622
ISSN: 1469-7793
0022-3751
DOI: 10.1111/j.1469-7793.2000.00613.x
Popis: In single perfused mesenteric microvessels of pithed frogs, we assessed wall strength from the critical pressure, PB, which has to be applied within the vessel in order to induce openings in the walls through which fluid and cells can extravasate. PB was determined in capillaries and venules of tissues at 12-20°C and after cooling to 0-5°C. The PB (mean ± s.e.m.) in 22 vessels between 12 and 20°C was 52.64 ± 3.86 cmH2O. In 19 microvessels cooled to less than 5°C, PB was 92.0 ± 7.40 cmH2O which was significantly higher than at room temperature (P < 0.001). The compliance of the vessel wall was estimated using both the red cell method and the oil meniscus technique. There was no measurable effect of temperature on wall compliance. The compliance of vessels from which the cells had been removed by previous perfusion with detergent solutions was very similar to that of intact vessels between 12 and 20°C and between 0 and 5°C. The negligible effects of temperature upon compliance suggest that microvessel walls have to be distended to a greater extent in cold tissue before PB is reached. This, together with their rapid closure, is consistent with the hypothesis that pressure-induced openings in microvascular walls are dependent on an active response of the endothelium rather than being the result of stress failure of the basement membrane. When the pressure in a closed-off capillary or venule is raised to a critical value, PB, gaps open in the vessel wall through which fluid and cells can extravasate into the tissues. The sudden development of these openings is usually interpreted as rupture or stress failure of the vessel wall (West et al. 1991). Since the wall strength of microvessels is believed to be determined by the basement membrane and surrounding interstitial tissue (e.g. Swayne et al. 1989), PB has been used to estimate the tensile strength of the basement membrane (West et al. 1991). Previously, we have reported that most of the openings which are induced by high pressures in frog mesenteric vessels pass through (rather than between) the endothelial cells (Neal & Michel, 1996a). Furthermore, the openings close when the pressure is lowered so that the permeability and strength of the vessel wall (as indicated by further estimates of PB) are recovered within a few minutes. The rapid recovery of wall strength suggests that the opening of gaps in a given microvessel at a particular value of PB might be related more to the properties of the endothelium than to those of its basement membrane. To explore this hypothesis we have exploited the reversibility of the phenomenon to examine how temperature affects the value of PB in single microvessels. We argued that if PB is determined primarily by the properties of the endothelium, then it might be expected to be changed conspicuously when tissue temperature is dropped by 10°C or more. If, on the other hand, PB is determined by the properties of the endothelial basement membrane, one might expect only a small effect of temperature on PB. When our results showed that PB was greatly increased at low tissue temperature, we realised that this effect might be secondary to a reduction in wall compliance. If openings were induced by a critical strain upon the wall, a higher pressure would be necessary to reach this level of strain in a stiffer vessel. To test this hypothesis, we examined the effects of lowering the tissue temperature on the compliance of microvessel walls and the contribution which the endothelial cells make towards compliance. Preliminary reports of some of the data in this paper have been presented to The Physiological Society (Neal & Michel, 1996b) and the British Microcirculation Society (Neal & Michel, 1996c).
Databáze: OpenAIRE
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