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Regulation of the Intracranial Fluids

Being encased in a rigid enclosure, the brain employs a sophisticated windkessel mechanism to regulate the flow of blood through the cerebral vascular bed [69-71]. This mechanism compensates for the transient increases in arterial blood volume entering the cranium that occur during systole, by displacing an approximately equal volume of CSF from the cranium into the spinal column [72]. As such, it ensures that the flow of blood through the cerebral capillary bed remains constant and non-pulsatile in healthy young adults [70], despite the considerable changes in the arterial blood flow rate entering the cranium that occur throughout the cardiac cycle (CC). The whole system is driven by volumetric changes in the arterial pulse, which are transferred to the CSF, causing it to pulse backwards and forwards across the foramen magnum (FM) (Fig.13.1). During systole the CSF travels in the caudal direction, whereas in diastole the flow is reversed, with the CSF travelling into the subarachnoid space (SAS) and interacting with the cortical bridging veins [73, 74].

While the presence of an intracranial windkessel mechanism is generally accepted, the arteriovenous time delay [75, 76] between peak arterial flow entering the cranium and peak venous flow leaving the cranium (Fig. 13.2a) has remained something of a mystery. The cranium is a rigid container filled with incompressible gel-like matter and fluids [77, 78]. Any increase in the intracranial arterial volume should therefore in theory be matched by an instantaneous displacement of fluid out of the cranium. While the displacement of CSF through the FM is virtually instantaneous [73, 74], the delay between the cervical arterial and venous flow rate peaks [75, 76] suggests that complex fluid interactions must be occurring within the cranium. Recently, a model was developed which sheds new light on the complex fluid interactions that occur within the cranium during the CC [79]. This model interprets the cervical blood and CSF flows in the neck to determine the temporal changes that occur in the intracranial arterial, venous and CSF volumes. It is illustrated in Fig. 13.2b, which shows the results of applying the model to mean cervical blood and CSF flow data (Fig. 13.2a) collected from 12 healthy young adults [80]. From this it can be seen that there is a strong inverse relationship between the arterial and CSF fluid volumes in the cranium. As arterial blood accumulates in the cranium during systole, so it displaces CSF, with the result that the intracranial CSF volume reduces to a minimum when the intracranial arterial volume is at its maximum. Conversely, during diastole, as the arterial blood flow entering the cranium decreases, so the returning CSF displaces arterial blood stored in the pial arteries, with the result that the intracranial CSF volume reaches a maximum at approximately the same time as the intracranial arterial blood volume is at its minimum. From Fig. 13.2b, it can be seen that during diastole, as the intracranial CSF volume increases, so venous blood starts to accumulate within the cranium. Only when the intracranial CSF volume has peaked and starts to decrease does the stored venous blood start to discharge from the cranium, suggesting that venous outflow is regulated in some way by the interaction between the CSF in the SAS and the cortical bridging veins, as Greitz [81] and Nakagawa et al. [82] postulated.

The timing of the intracranial fluid regulatory mechanism appears critical. In late diastole and early systole, the cranium can only accommodate the stored venous

Hydrodynamic model of the brain, showing the interactions between the arterial and venous blood flows and the cerebrospinal fluid

Fig. 13.1 Hydrodynamic model of the brain, showing the interactions between the arterial and venous blood flows and the cerebrospinal fluid (CSF). SSS superior sagittal sinus, STS straight sinus, SAS subarachnoid space, AVarachnoid villi, CP choroid plexus, FM foramen magnum, WM windkessel mechanism, SR Starling resistor, VL lateral ventricle, V3 third ventricle, V4 fourth ventricle, AoS aqueduct of Sylvius, IJVinternal jugular vein, VV vertebral veins

blood because the store of arterial blood in the cranium is depleted during this period. Similarly, the system requires the free egress of venous blood of the cranium during systole. A number of studies have shown that constriction of the internal jugular veins (IJVs) causes increased retention of blood in the cerebral veins [83] and that this can increase the stiffness of the brain parenchyma [2], causing the amplitude of the CSF pulse in the aqueduct of Sylvius (AoS) to increase [2, 3]. Furthermore, rotation of the head can compress both the IJVs and the vertebral veins [84] inhibiting cerebral venous drainage, something that has been shown to increase the venous pressure in the confluens sinuum by as much as 30.3% [85]. This in turn can influence ICP. Indeed, it has been shown that in anaesthetised neurosurgical patients lying on a flat surface, the ICP can be raised by 4.1-4.8 mmHg simply through rotation of the head [86]. Collectively, these findings suggest that

(a) Mean cervical arterial, venous and cerebrospinal fluid

Fig. 13.2 (a) Mean cervical arterial, venous and cerebrospinal fluid (CSF) flow rates over a cardiac cycle, for all 12 subjects aggregated together. (NB. For ease of representation, the venous signal has been inverted.) (b) Mean intracranial arterial, venous and CSF volumetric changes over the cardiac cycle, for all 12 subjects aggregated together (Adapted from Beggs et al. [80])

the characteristics of the cerebral venous drainage system can influence fluid dynamics within the cranium.

 
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