Cerebrospinal fluid dynamics in the human cranial subarachnoid space: an overlooked mediator of cerebral disease. I. Computational model

Abstract

Abnormal cerebrospinal fluid (CSF) flow is suspected to be a contributor to the pathogenesis of neurodegenerative diseases such as Alzheimer's through the accumulation of toxic metabolites, and to the malfunction of intracranial pressure regulation, possibly through disruption of neuroendocrine communication. For the understanding of transport processes involved in either, knowledge of in vivo CSF dynamics is important. We present a three-dimensional, transient, subject-specific computational analysis of CSF flow in the human cranial subarachnoid space (SAS) based on in vivo magnetic resonance imaging. We observed large variations in the spatial distribution of flow velocities with a temporal peak of 5 cm s(-1) in the anterior SAS and less than 4 mm s(-1) in the superior part. This could reflect dissimilar flushing requirements of brain areas that may show differences in susceptibility to pathological CSF flow. Our methods can be used to compare the transport of metabolites and neuroendocrine substances in healthy and diseased brains.

Figure 1.

(a) Anatomic MRI images of the cranial space; (b) segmentation and reconstruction of the SAS and the brain structures; (c) three-dimensional brain anatomy; (d) three-dimensional SAS anatomy; (e) detailed anatomy of the SAS showing sulci.

Figure 2.

(a) Rendering of the cranial SAS (opaque) and of the superior spinal SAS and fourth ventricle (transparent). (b) Cranial SAS novel to this work.

Figure 3.

Velocities measured with MRI normal to the boundaries in (a) cerebellomedullary cistern and (b) pontine cistern during one cardiac cycle of period T. Velocities are shown at uniform intervals of T/5.

Figure 4.

Spatially averaged transient deformation rate of the cranial SAS at the brain surface and the corresponding volumetric flow rate used as the boundary condition.

Figure 5.

Relative pressure, P, contours in the SAS during one complete cardiac cycle. The pressure values are given with respect to the CSF outlet pressure, P_CSF,outlet = ΔP_AG + P_SSS, where P_SSS is the blood pressure in the superior sagittal sinus and ΔP_AG is the pressure drop across the AGs.

Figure 6.

Velocity magnitude contours at cross sections of the cranial SAS at selected points in time within one cardiac cycle. Also shown are the stream traces of virtual massless particles injected arbitrarily within the domain at different points in time.