Critical Closing Pressure and Cerebrovascular Resistance Responses to Intracranial Pressure Variations in Neurocritical Patients

Abstract

Background: Critical closing pressure (CrCP) and resistance-area product (RAP) have been conceived as compasses to optimize cerebral perfusion pressure (CPP) and monitor cerebrovascular resistance, respectively. However, for patients with acute brain injury (ABI), the impact of intracranial pressure (ICP) variability on these variables is poorly understood. The present study evaluates the effects of a controlled ICP variation on CrCP and RAP among patients with ABI.

Methods: Consecutive neurocritical patients with ICP monitoring were included along with transcranial Doppler and invasive arterial blood pressure monitoring. Internal jugular veins compression was performed for 60 s for the elevation of intracranial blood volume and ICP. Patients were separated in groups according to previous intracranial hypertension severity, with either no skull opening (Sk1), neurosurgical mass lesions evacuation, or decompressive craniectomy (DC) (patients with DC [Sk3]).

Results: Among 98 included patients, the correlation between change (Δ) in ICP and the corresponding ΔCrCP was strong (group Sk1 r = 0.643 [p = 0.0007], group with neurosurgical mass lesions evacuation r = 0.732 [p < 0.0001], and group Sk3 r = 0.580 [p = 0.003], respectively). Patients from group Sk3 presented a significantly higher ΔRAP (p = 0.005); however, for this group, a higher response in mean arterial pressure (change in mean arterial pressure p = 0.034) was observed. Exclusively, group Sk1 disclosed reduction in ICP before internal jugular veins compression withholding.

Conclusions: This study elucidates that CrCP reliably changes in accordance with ICP, being useful to indicate ideal CPP in neurocritical settings. In the early days after DC, cerebrovascular resistance seems to remain elevated, despite exacerbated arterial blood pressure responses in efforts to maintain CPP stable. Patients with ABI with no need of surgical procedures appear to remain with more effective ICP compensatory mechanisms when compared with those who underwent neurosurgical interventions.

Trial registration: ClinicalTrials.gov NCT03694678.

Keywords: Acute brain injury; Cerebral perfusion pressure; Critical closing pressure; Intracranial compliance; Intracranial pressure; Resistance-area product.

Fig. 1

Population average of cerebral hemodynamic parameters following temporary compression of the internal jugular vein in patients with traumatic brain injury. The vertical black arrow marks the beginning of compression. a Mean arterial blood pressure (MAP); b cerebral blood velocity; c intracranial pressure (ICP), with notably spontaneous ICP lowering after 20 s of IJVC (interval between red arrows) exclusively for group Sk1; d critical closing pressure (CrCP); e cerebral perfusion pressure (CPP) (CPP = MAP − ICP); and f resistance-area product (RAP). Representation corresponds to group Sk1 (undamaged skull, continuous line, n = 23), group Sk2 (craniotomy, dotted line, n = 35), and group Sk3 (decompressive craniectomy, dashed line, n = 22). The error bars represent ± 1 SE at the time of occurrence. BP, blood pressure; CBFV, cerebral blood flow velocity; IJVC, internal jugular veins compression; SE, standard error of the mean

Fig. 2

Change in critical closing pressure (CrCP) as a function of the change in intracranial pressure (ICP) resulting from temporary compression of the internal jugular vein. Linear regression lines with raw data correspond to patients with a undamaged skull (circles, r = 0.643, p = 0.0007), b craniotomy (open squares, r = 0.762, p < 0.0001), and c craniectomy (crosses, r = 0.580, p = 0.003). d Comparison of regression lines corresponding to undamaged skull (dashed line), craniotomies (dotted line), and craniectomy (solid line)

Fig. 3

Population average (n = 37) of cerebral hemodynamic parameters following temporary compression of the internal jugular vein in patients with unilateral traumatic brain injury. The vertical arrow marks the beginning of compression. a Mean arterial blood pressure (MABP); b cerebral blood flow velocity (CBFV); c intracranial pressure (ICP); d critical closing pressure (CrCP); e cerebral perfusion pressure (CPP) (CPP = MABP − ICP); and f resistance-area product (RAP). Continuous line indicates measurements from the affected hemisphere, dashed line from the nonaffected hemisphere. The error bars represent ± 1 SE at the time of occurrence. SE, standard error of the mean

Fig. 4

Representative changes in cerebral hemodynamic parameters in a 41-year-old male patient with right traumatic craniotomy for hematoma evacuation. The vertical arrow marks the beginning of jugular veins compression. a Mean arterial blood pressure (MABP); b cerebral blood flow velocity (CBFV); c intracranial pressure (ICP); d critical closing pressure (CrCP); e cerebral perfusion pressure (CPP = MABP − ICP); and f resistance-area product (RAP). Continuous line indicates measurements from the right hemisphere, dashed line from the left hemisphere. ICP was high at the baseline (~ 28 mm Hg) but positively compensated with MABP elevation during compression, leading CPP to not drop lower than 55 mm Hg. CBFV dropped bilaterally but remained under standard values. CrCP elevation was uniform for both hemispheres, whereas RAP elevation was sensitive for the affected (right) hemisphere. BP, blood pressure