Alterations of mechanical properties in canine basilar arteries after subarachnoid hemorrhage

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✓ The purpose of this study was to examine the hypotheses that structural stiffening of the arterial wall contributes to chronic cerebral vasospasm, and that alteration in properties of smooth muscle takes place after subarachnoid hemorrhage (SAH). Subarachnoid hemorrhage and subsequent chronic vasospasm were induced in dogs by two cisternal injections of autologous blood (on Day 0 and Day 2). Vasospasm was confirmed by angiography performed on Day 0 and Day 7. Animals in the control group underwent angiography only. On Day 8, the mechanical properties of the basilar arteries were studied in vitro. Passive compliance, measured under total inhibition of spontaneous myogenic tone with diltiazem (10−4 M) plus papaverine (10−4 M) was smaller in the SAH group. The length-contraction curve was shifted to the left and the optimum length for maximum contraction (Lmax) was significantly shorter in the spastic blood vessels. The spontaneous myogenic tone was augmented in the SAH group, resulting in an increase in resting tension at each length. By contrast, the maximum contractions in response to KCl and uridine 5′-triphosphate were markedly reduced in the SAH group, without changes in sensitivity to these agents. These differences in mechanical properties were observed in rings both with and without endothelium. The results indicate that, in chronic vasospasm, stiffening of the noncontractile component of the vasculature takes place as well as alterations in the contractile component, both of which presumably contribute to the shift in resting length-tension relationship and length-contraction relationship of the artery. The decreased distensibility, the increase in resting tension, and the shortening of the Lmax all favor a smaller diameter of the artery after SAH, possibly contributing to vasospasm.

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Address reprint requests to: Phyo Kim, M.D., Ph.D., Department of Neurologic Surgery, Mayo Clinic, Rochester, Minnesota 55905.

© AANS, except where prohibited by US copyright law.

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Figures

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    Light micrographs of basilar artery rings from a subarachnoid hemorrhage group dog after completion of an organ chamber experiment: rings with endothelium (A: × 640, B: × 100); and rings without endothelium (C: × 640, D: × 100). Note that the internal elastica lamina and the layers below including the adventitia are well maintained in the rings without endothelium. H & E.

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    Passive compliance in rings with endothelium (see Materials and Methods section for the calculation of compliance). Open bars represent data from the control group, and shaded bars represent those from the subarachnoid hemorrhage (SAH) group. Data were measured in the presence of diltiazem (10−4 M) and papaverine (10−4 M) to suppress the active myogenic contraction. Data are shown as means ± standard error of the means for eight specimens. The asterisks indicate a statistically significant difference between the two groups (p < 0.05, Student's unpaired t-test).

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    Passive compliance in rings without endothelium, in the control group (open bars) and in the subarachnoid hemorrhage (SAH) group (shaded bars). Compliance was measured in the presence of diltiazem (10−4 M) and papaverine (10−4 M). Single asterisks indicate a significant difference between the control and the subarachnoid hemorrhage groups (p < 0.05, Student's unpaired t-test). Double asterisks indicate a significant difference between rings with and those without endothelium in each group. Data are shown as means ± standard error of the means in eight specimens.

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    A: Length-contraction relationship to uridine 5′-triphosphate (UTP, 10−5 M) during progressive stepwise stretch in rings with endothelium. Open bars represent data from the control group and shaded bars represent those from the subarachnoid hemorrhage group. Initially, the rings were equilibrated for 30 minutes at a length where the tension started to increase measurably, which is referred to as the initial length. B: Resting length-tension relationship in rings with endothelium in the control (open bars) and in the subarachnoid hemorrhage groups (shaded bars). The asterisks indicate a significant difference in tension between the two groups (p < 0.05, Student's unpaired t-test). Data in A and B are shown as means ± standard error of the means of recordings made in 32 rings (four rings from each of eight different animals).

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    Maximum contraction in the presence of KCl in rings with and without endothelium in the control (open bars) and subarachnoid hemorrhage (SAH) groups (shaded bars). Measurements were made at optimum length in each ring. Data are presented as means ± standard error of the means for 32 rings (four rings from each of eight different animals). The asterisks indicate a significant difference between the two groups (p < 0.05, Student's unpaired t-test).

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    Concentration-response relationship to KCl in rings with (filled symbols) or without (open symbols) endothelium. Responses were expressed as a percentage of the maximum contraction in the presence of KCl in each ring. Circles indicate data from the control group and squares indicate those from the subarachnoid hemorrhage (SAH) group. Data are shown as means ± standard error of the means in eight rings.

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    Contraction in response to uridine 5′-triphosphate (UTP, 10−5 M) in rings with or without endothelium from the control group (open bars) and the subarachnoid hemorrhage (SAH) group (shaded bars). Contractions were measured at optimum length in each ring. Data are expressed as means ± standard error of the means for 32 rings (four rings from each of eight different animals). The asterisks indicate a significant difference between the two groups (p < 0.05, Student's unpaired t-test).

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    Concentration-response curve in the presence of uridine 5′-triphosphate (UTP) in rings with (filled symbols) and without (open symbols) endothelium. Responses were expressed as a percentage of the maximum contraction to KCl. Circles represent data from the control group, and squares represent those from the subarachnoid hemorrhage (SAH) group. The asterisks indicate a significant difference between the two groups (p < 0.05, Student's unpaired t-test). Data are presented as means ± standard error of the means for eight rings.

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