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The mechanical properties of the aorta of the cephalopod mollusc, Octopus dofleini (Wulker) Shadwick, Robert Edward


In any circulatory system, the mechanical properties of the walls of the arteries will have significant effects on the dynamics of blood flow. The distensibi1ity of the artery wall is important in determining the wave propagation characteristics of the system, as well as contributing a pulse smoothing effect on the intermittant flow of blood from the heart. These properties are well studied in mammalian circulatory systems, but have never been directly investigated in any invertebrate animal. This study examines the structure and mechanical properties of the major artery in a cephalopod mollusc, Octopus dofleini, and relates these properties to cardiovascular dynamics in the living animal. The dorsal aorta of cephalopods is the large blood vessel through which blood flows from the systemic heart. The walls of this artery are comprised of thick layers of circularly and longitudinally oriented muscle cells. Outside the muscle layers is a loose collagenous adventitia. Innermost, adjacent to the lumen is a layer of elastic fibres, analogous to vertebrate elastin fibres. In addition, these fibres extend throughout the artery wall as a network of extracellular connective tissue. The elastic fibres have been isolated from the octopus aorta and subjected to direct mechanical and chemical tests. These fibres are composed of a protein which has rubber-like properties, that is, the material has high extensibility and a modulus of elasticity, G (= 4.65 X 10⁵ N/m² ), which is similar to a rubber. Chemical and optical properties of this unusual protein suggest that the molecular structure is one of covalently crosslinked, random coil, kinetically free chains. This interpretation is consistent with the thermoelastic data for these protein fibres which fit closely the predictions of the kinetic theory of entropic elasticity in rubbers. In vitro mechanical tests on the octopus aorta showed that this vessel is a highly distensible, resilient elastic tube which, like mammalian arteries, becomes much less compliant as it is extended. The tangential elastic modulus in the circumferential direction (Ec) ranged from 9X10³ to 2X10⁵ N/m² over the normal resting range of physiological pressures (20 to 50 cm of water), while the elastic modulus in the longitudinal direction (El) was always about one-half of Ec. Hysteresis in quasi-static inflations was about 25%. The dynamic modulus of elasticity increased continuously with frequencies from 0.1 Hz to 10Hz. Tan d varied from about 0.10 to 0.15 over the physiologically relevant range of frequencies in this animal (0.1 to 1.0 Hz). These results show that this artery can function as an elastic, pulse smoothing component in the octopus circulation. Further, it appears that the elastic properties of the intact artery can be attributed largely to the rubber-like protein found in the wall. In vivo measurements of blood pressure and flow in the octopus show an impedance spectrum which is similar to what has been observed in turtles and frogs, that is, the arterial circulation of this invertebrate is adequately described by a simple Windkessel model. Pulse wave velocity measured in vivo appeared to be greater than 10 m/sec, although the velocity predicted from the elastic properties of the aorta was less than 5 m/sec. These anomalies arise because, due to the low heart rate of the octopus, the length of the aorta is less than 5% of the wavelength of the significant frequencies in the pressure pulse. The arterial system of the octopus is one which is dominated by strong wave reflections, but does not exhibit other transmission effects such as peaking and distortion of the travelling pressure wave. These results may have general application to other cephalopods, but it will be interesting to examine species, such as pelagic squids, which presumably have higher blood pressure and heart rates.

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