Effect of increased positive end-expiratory pressure on intracranial pressure and cerebral oxygenation: impact of respiratory mechanics and hypovolemia

Abstract

Background: To evaluate the impact of positive end-expiratory pressure (PEEP) on intracranial pressure (ICP) in animals with different respiratory mechanics, baseline ICP and volume status.

Methods: A total of 50 male adult Bama miniature pigs were involved in four different protocols (n = 20, 12, 12, and 6, respectively). Under the monitoring of ICP, brain tissue oxygen tension and hemodynamical parameters, PEEP was applied in increments of 5 cm H2O from 5 to 25 cm H2O. Measurements were taken in pigs with normal ICP and normovolemia (Series I), or with intracranial hypertension (via inflating intracranial balloon catheter) and normovolemia (Series II), or with intracranial hypertension and hypovolemia (via exsanguination) (Series III). Pigs randomized to the control group received only hydrochloride instillation while the intervention group received additional chest wall strapping. Common carotid arterial blood flow before and after exsanguination at each PEEP level was measured in pigs with intracranial hypertension and chest wall strapping (Series IV).

Results: ICP was elevated by increased PEEP in both normal ICP and intracranial hypertension conditions in animals with normal blood volume, while resulted in decreased ICP with PEEP increments in animals with hypovolemia. Increasing PEEP resulted in a decrease in brain tissue oxygen tension in both normovolemic and hypovolemic conditions. The impacts of PEEP on hemodynamical parameters, ICP and brain tissue oxygen tension became more evident with increased chest wall elastance. Compare to normovolemic condition, common carotid arterial blood flow was further lowered when PEEP was raised in the condition of hypovolemia.

Conclusions: The impacts of PEEP on ICP and cerebral oxygenation are determined by both volume status and respiratory mechanics. Potential conditions that may increase chest wall elastance should also be ruled out to avoid the deleterious effects of PEEP.

Keywords: Cerebral blood flow; Cerebral oxygenation; Hypovolemia; Intracranial pressure; Positive end-expiratory pressure; Respiratory mechanics.

Conflict of interest statement

The authors declare that they have no competing interests

© 2021. The Author(s).

Figures

Fig. 1

The impacts of positive end-expiratory pressure in animals with normovolemia and normal intracranial pressure (Series I, n = 10 per group): Data were presented as mean and standard deviation. RM-ANOVA was used. The corresponding changes of mean arterial pressure were presented in grey lines (showing means only), solid line: control group, dash line: chest wall strapping group. A ICP significantly increased when PEEP was increased (p < 0.001 for both groups), and the magnitude was significantly higher in the chest wall strapping group than in the control group (p = 0.014). B PtiO2 significantly decreased when PEEP was increased (p < 0.001 for both groups), but the magnitude was similar between groups (p = 0.927). C CO significantly decreased with PEEP increment (p < 0.001 for both groups), while no difference was observed between groups (p = 0.907). D CPP significantly decreased with PEEP increment (p < 0.001 for both groups), no difference was observed between groups (p = 0.645). ICP intracranial pressure, PEEP positive end-expiratory pressure, PtiO2 brain tissue O2 tension, CO cardiac output, CPP cerebral perfusion pressure

Fig. 2

The impacts of positive end-expiratory pressure in animals with normovolemia and intracranial hypertension (Series II, n = 6 per group). Data were presented as mean and standard deviation. RM-ANOVA was used. The corresponding changes of mean arterial pressure were presented in grey lines (showing means only), solid line: control group, dash line: chest wall strapping group. A ICP significantly increased when PEEP was increased (p < 0.001 for both groups), and the magnitude was significantly higher in the chest wall strapping group than in the control group (p = 0.022). B PtiO2 significantly decreased when PEEP was increased (p < 0.001 for both groups), but the magnitude was similar between groups (p = 0.333). C CO significantly decreased with PEEP increment (p < 0.001 for both groups), while no difference was observed between groups (p = 0.649). D CPP significantly decreased with PEEP increment (p < 0.001 for both groups), no difference was observed between groups (p = 0.367). ICP intracranial pressure, PEEP positive end-expiratory pressure, PtiO2 brain tissue O2 tension, CO cardiac output, CPP cerebral perfusion pressure

Fig. 3

The impacts of positive end-expiratory pressure in animals with hypovolemia and intracranial hypertension (Series III, n = 6 per group). Data were presented as mean and standard deviation. RM-ANOVA was used. The corresponding changes of mean arterial pressure were presented in grey lines (showing means only), solid line: control group, dash line: chest wall strapping group. A ICP significantly decreased when PEEP was increased (p < 0.001 for both groups), and the magnitude was significantly greater in the chest wall strapping group than in the control group (p = 0.018). B PtiO2 decreased when PEEP was increased (p < 0.001 for both groups), and the magnitude was greater in the chest wall strapping group than in the control group (p = 0.020). C CO significantly decreased with PEEP increment (p < 0.001 for both groups), there was a significantly greater decrease in CO in the chest wall strapping group than in the control group (p = 0.020). D CPP significantly decreased with PEEP increment (p < 0.001 for both groups), no difference was observed between groups (p = 0.205). ICP intracranial pressure, PEEP positive end-expiratory pressure, PtiO2 brain tissue O2 tension, CO cardiac output, CPP cerebral perfusion pressure

Fig. 4

The impacts of positive end-expiratory pressure on common carotid arterial blood flow (Series IV, n = 6). Data were presented as mean and standard deviation. RM-ANOVA was used. The corresponding changes of mean arterial pressure were presented in grey lines (showing means only), solid line: pre-exsanguination, dash line: post-exsanguination. A Common carotid arterial blood flow decreased significantly when PEEP was increased (p < 0.001 for both conditions), and the magnitude was significantly greater in the post-exsanguination (i.e., hypovolemic) condition than in the pre-exsanguination (i.e., normovolemic) condition (p < 0.001). B CO significantly decreased with PEEP increment (p < 0.001 for both conditions), there was a significantly greater decrease in CO in the post-exsanguination condition than in the pre-exsanguination condition (p < 0.001). PEEP positive end-expiratory pressure, CO cardiac output