Cerebrospinal fluid hydrodynamics in type I Chiari malformation

Abstract

Purpose: The objective of this study was to review past studies that have used engineering analysis to examine cerebrospinal fluid hydrodynamics in cranial and spinal subarachnoid spaces in both healthy humans and those affected by type I Chiari malformation.

Methods: A PubMed search of literature pertaining to cerebrospinal fluid hydrodynamics was performed with a particular focus on those that utilized methods such as computational fluid dynamics or experimental flow modeling.

Discussion: From the engineer's perspective, type I Chiari malformation is an abnormal geometry of the cerebellum that causes increased resistance to cerebrospinal fluid flow between the intracranial and spinal subarachnoid space. As such, understanding the hydrodynamics of cerebrospinal fluid in the craniospinal subarachnoid space has long been thought to be important in the diagnosis and management of type I Chiari malformation. Hydrodynamic quantification of cerebrospinal fluid motion in the subarachnoid space may better reflect the pathophysiology of the disorder and serve as a prognostic indicator in conjunction with geometric magnetic resonance measurements that are currently used clinically. This review discusses the results of studies that have sought to quantify the hydrodynamics of cerebrospinal fluid motion using computational and experimental modeling and critiques the methods by which the results were obtained.

Conclusion: Researchers have found differences in cerebrospinal fluid velocities and pressures in type I Chiari malformation patients compared to healthy subjects. However, further research is necessary to determine the causal relationship between changes to hydrodynamic parameters such as cerebrospinal fluid velocity, pressure, resistance to flow, and craniospinal compliance and clinical aspects such as neurological symptoms, radiological evidence of severity, and surgical success.

Figure 1

T2-weighted sagittal magnetic resonance images of the head and cervical spine (above) and three-dimensional reconstruction of the cervical spinal subarachnoid space near the foramen magnum (below). (A) Healthy subject; (B) patient with symptomatic type I Chiari malformation.

Figure 2

Type I Chiari malformation is characterized by both the altered neural anatomy and cerebrospinal fluid (CSF) dynamics. Presently, it is unclear which of these directly cause the symptoms and/or neural tissue damage that patients experience.

Figure 3

Velocity traces are shown for each voxel of an axial plane phase-contrast magnetic resonance image sequence taken from a patient with type I Chiari malformation over the cardiac cycle by Quigley et al. White traces represent voxels that exhibited cephalad velocities in excess of 40 mm/s (velocity jets). Green traces represent voxels that exhibited caudad velocities during most of the cardiac cycle. Red traces represent voxels with low-magnitude (<30 mm/s) cephalad velocities. The spatial mean velocity is shown as a heavy white trace for reference. These traces demonstrate the inhomogeneous distribution of velocities that can occur in the spinal canal of a patient with type I Chiari malformation.

Figure 4

Phase-contrast magnetic resonance images of the pulsatile cerebrospinal fluid velocity observed during systole (left) and diastole (right) and with the corresponding velocity distribution at the location indicated by the white dotted line from Loth et al. This demonstrates the blunt velocity profile that would typically be observed in the healthy spinal canal.

Figure 5

Geometric sketches of the idealized healthy spinal subarachnoid space geometries used for lattice-Boltzmann simulations of cerebrospinal fluid flow by Stockman. Shaded areas represent solid structures. Model A is an open elliptical annular cavity, where the central ellipse represents the spinal cord. Model B adds nerve bundles on the side of the cord (thick lines) and a regularly distributed array of trabeculae on the dorsal and ventral sides of the cord (thin lines). Model C adds a denticulate ligament on the lateral sides of the cord. Model D is like B, but the trabeculae positions are randomized. Though obstructions to flow increase with each model, very little change to the flow field was observed.

Figure 6

Stream traces colored by velocity magnitude from computational fluid dynamics model of the inferior cranial and superior spinal subarachnoid spaces of a healthy subject geometry by Gupta et al. demonstrating the three-dimensional complexity of cerebrospinal fluid motion in that region. Tracer particles were injected at Plane A, which intersected the basal pontine and cerebellomedullary cisterns.

Figure 7

Cerebrospinal fluid velocity patterns obtained from a computational fluid dynamics simulation by Roldan et al. of flow at peak systole in six different axial levels in a healthy model (left column) and a type I Chiari malformation-affected model (right column) under steady flow conditions. Colors indicate the magnitude of the axial velocity (caudad direction); arrows indicate the directions and magnitudes of secondary velocities (anterior, medial, or posterior direction).