Higher intracranial pressure variability is associated with lower cerebrovascular resistance in aneurysmal subarachnoid hemorrhage

Abstract

Higher intracranial pressure variability (ICPV) has been associated with a more favorable cerebral energy metabolism, lower rate of delayed ischemic neurologic deficits, and more favorable outcome in aneurysmal subarachnoid hemorrhage (aSAH). We have hypothesized that higher ICPV partly reflects more compliant and active cerebral vessels. In this study, the aim was to further test this by investigating if higher ICPV was associated with lower cerebrovascular resistance (CVR) and higher cerebral blood flow (CBF) after aSAH. In this observational study, 147 aSAH patients were included, all of whom had been treated in the Neurointensive Care (NIC) Unit, Uppsala, Sweden, 2012-2020. They were required to have had ICP monitoring and at least one xenon-enhanced computed tomography (Xe-CT) scan to study cortical CBF within the first 2 weeks post-ictus. CVR was defined as the cerebral perfusion pressure in association with the Xe-CT scan divided by the concurrent CBF. ICPV was defined over three intervals: subminute (ICPV-1m), 30-min (ICPV-30m), and 4 h (ICPV-4h). The first 14 days were divided into early (days 1-3) and vasospasm phase (days 4-14). In the vasospasm phase, but not in the early phase, higher ICPV-4h (β = - 0.19, p < 0.05) was independently associated with a lower CVR in a multiple linear regression analysis and with a higher global cortical CBF (r = 0.19, p < 0.05) in a univariate analysis. ICPV-1m and ICPV-30m were not associated with CVR or CBF in any phase. This study corroborates the hypothesis that higher ICPV, at least in the 4-h interval, is favorable and may reflect more compliant and possibly more active cerebral vessels.

Keywords: Aneurysmal subarachnoid hemorrhage; Cerebral blood flow; Cerebrovascular resistance; Intracranial pressure variability; Xenon-enhanced computed tomography.

Fig. 1

ICPV measures—example from one patient. The figure demonstrates the temporal course of ICPV in one patient over an hour of monitoring in association to a Xe-CT scan (time-point 00:30). ICPV-1m exhibited some temporal variation, whereas ICPV-4h was stable around 1 mmHg. ICP intracranial pressure, ICPV ICP variability, Xe-CT xenon-enhanced computed tomography

Fig. 2

Cortical cerebral blood flow measurement—one example. The figure demonstrates cortical CBF in 20 different ROIs in a Xe-CT image. Global CBF was calculated based on average cortical CBF of typically three Xe-CT slices from the scan. Red areas indicate high CBF and blue areas low CBF. CBF cerebral blood flow, ROI region of interest, Xe-CT xenon-enhanced computed tomography

Fig. 3

A–D ICPV-4h in relation to CBF and CVR in the early phase and the vasospasm phase. These scatter plots demonstrate the association between ICPV-4h and global cortical CBF in the early phase (A) and the vasospasm phase (B) as well as with CVR in the early phase (C) and in the vasospasm phase (D). Higher ICPV-4h was significantly associated with higher CBF (r = 0.19, p < 0.05) and lower CVR (r =  − 0.20, p < 0.05) in the vasospasm phase. CBF cerebral blood flow, CVR cerebrovascular resistance, ICPV intracranial pressure variability

Fig. 4

ICP variability—explanatory variables. We have previously demonstrated [5] that higher ICPV depends on variations in CBV as a consequence of higher BPV and likely also active and compliant cerebral vessels. The effect of the CBV variations on ICPV are amplified in a state of low intracranial compliance and high ICP. Hence, the suggested beneficial underlying mechanism of higher ICPV is supposed to be more active and compliant cerebral vessels predisposing for better CBF regulation and cerebral energy metabolic supply [3]