The Impact of Spinal Cord Nerve Roots and Denticulate Ligaments on Cerebrospinal Fluid Dynamics in the Cervical Spine

Soroush Heidari Pahlavian,Alexander C Bunck,R Shane Tubbs,Bryn A Martin,Mark Goodin,Mehrdad Raisee,Theresia Yiallourou,Francis Loth,Kristel Sleegers

doi:10.1371/journal.pone.0091888

Abstract

Cerebrospinal fluid (CSF) dynamics in the spinal subarachnoid space (SSS) have been thought to play an important pathophysiological role in syringomyelia, Chiari I malformation (CM), and a role in intrathecal drug delivery. Yet, the impact that fine anatomical structures, including nerve roots and denticulate ligaments (NRDL), have on SSS CSF dynamics is not clear. In the present study we assessed the impact of NRDL on CSF dynamics in the cervical SSS. The 3D geometry of the cervical SSS was reconstructed based on manual segmentation of MRI images of a healthy volunteer and a patient with CM. Idealized NRDL were designed and added to each of the geometries based on in vivo measurments in the literature and confirmation by a neuroanatomist. CFD simulations were performed for the healthy and patient case with and without NRDL included. Our results showed that the NRDL had an important impact on CSF dynamics in terms of velocity field and flow patterns. However, pressure distribution was not altered greatly although the NRDL cases required a larger pressure gradient to maintain the same flow. Also, the NRDL did not alter CSF dynamics to a great degree in the SSS from the foramen magnum to the C1 level for the healthy subject and CM patient with mild tonsillar herniation (∼6 mm). Overall, the NRDL increased fluid mixing phenomena and resulted in a more complex flow field. Comparison of the streamlines of CSF flow revealed that the presence of NRDL lead to the formation of vortical structures and remarkably increased the local mixing of the CSF throughout the SSS.

Highlights

99 years ago, neurosurgeon Harvey Cushing wrote in his seminal manuscript on cerebrospinal fluid (CSF) studies, ‘‘Our knowledge of the meningeal and ependymal coverings of the central nervous system, as well as of the part played by the fluid which circulates through and over them, has hardly kept pace with our knowledge of the nervous tissues which they envelop.’’ To this day, the complete physiological importance of the CSF dynamics remains enigmatic
This study aims to determine the impact of nerve roots and denticulate ligaments (NRDL) on CSF dynamics using anatomically realistic 3D computational fluid dynamics (CFD) models of the cervical spine
The CFD model was based on subject specific MRI measurements of flow and geometry in the cervical spine obtained for a healthy subject and a Chiari malformation (CM) patient

Summary

Introduction

99 years ago, neurosurgeon Harvey Cushing wrote in his seminal manuscript on cerebrospinal fluid (CSF) studies, ‘‘Our knowledge of the meningeal and ependymal coverings of the central nervous system, as well as of the part played by the fluid which circulates through and over them, has hardly kept pace with our knowledge of the nervous tissues which they envelop.’’ To this day, the complete physiological importance of the CSF dynamics remains enigmatic. Researchers have analyzed SSS CSF velocities in vivo [1,14,15], in vitro [16,17,18] and utilizing computational fluid dynamics (CFD) simulations in silico [19,20,21,22]. These efforts have given valuable information about the CSF movement with the long-term goal of determining objective and quantitative measures of disease severity

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Conclusion