The influence of the relative timing of arterial and subarachnoid space pulse waves on spinal perivascular cerebrospinal fluid flow as a possible factor in syrinx development

Laboratory investigation

Restricted access

Object

The mechanisms of syringomyelia have long puzzled neurosurgeons and researchers alike due to difficulties in identifying the driving forces behind fluid flow into a syrinx, apparently against a pressure gradient between the spinal cord and the subarachnoid space (SAS). Recently, the synchronization between CSF flow and the cardiac cycle has been postulated to affect fluid flow in the spinal cord. This study aims to determine the effect of changes in the timing of SAS pressure on perivascular flow into the spinal cord.

Methods

This study uses a computational fluid dynamics model to investigate whether the relative timing of a spinal artery cardiovascular pulse wave and fluid pressure in the spinal SAS can influence CSF flow in the perivascular spaces.

Results

The results show that the mass flow rate of CSF through a model periarterial space is strongly influenced by the relative timing of the arterial pulse wave and the SAS pressure.

Conclusions

These findings suggest that factors that might alter the timing of the pulse wave or the fluid flow in the SAS could potentially affect fluid flow into a syrinx.

Abbreviations used in this paper: CM = Chiari malformation; PVS = perivascular space; SAS = subarachnoid space.

Article Information

Address correspondence to: Lynne E. Bilston, Ph.D., Prince of Wales Medical Research Institute, University of New South Wales, Corner Barker and Easy Streets, Randwick, New South Wales 2031, Australia. email: l.bilston@unsw.edu.au.

Please include this information when citing this paper: published online June 12, 2009; DOI: 10.3171/2009.5.JNS08945.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Schematic geometry of a PVS model. The top panel (A) shows the general location, and the 2 insets show the local area at the junction of the SAS and a penetrating artery and PVS that is modeled. The region in the lower circular inset corresponds to the model geometry as shown in B. The arrows in B represent the dimensions of various parts of the model. P = 0 represents pressure set to 0 in that location. PSAS(t) = time-varying pressure in the SAS. r = 75 μm indicates the radius of curvature of the pia mater where it attaches to the artery.

  • View in gallery

    Line graphs showing SAS pressure (upper) and arterial pulse wave (lower) over 1 second.

  • View in gallery

    Bar graph (upper) shows the mass flow rate through the PVS, depending on the relative timing of the arterial pulse wave and SAS pressure wave. The schematic illustration (lower) shows 2 scenarios with the peak SAS pressure wave arriving when arterial pressure is low (left), resulting in higher inflow (offset = ~ 0.5 seconds), and when arterial pressure is high (right), resulting in lower inflow (offset = ~ 0 seconds).

References

  • 1

    Ball MJDayan AD: Pathogenesis of syringomyelia. Lancet 2:7998011972

  • 2

    Bilston LEFletcher DFBrodbelt ARStoodley MA: Arterial pulsation-driven cerebrospinal fluid flow in the perivascular space: a computational model. Comput Methods Biomech Biomed Engin 6:2352412003

  • 3

    Bilston LEFletcher DFStoodley MA: Focal spinal arachnoiditis increases subarachnoid space pressure: a computational study. Clin Biomech (Bristol Avon) 21:5795842006

  • 4

    Bloomfield IGJohnson IHBilston LE: Effects of proteins, blood cells and glucose on the viscosity of cerebrospinal fluid. Pediatr Neurosurg 28:2462511998

  • 5

    Brodbelt ARStoodley MAJones NRNontraumatic syringomyelia. Clark CR: The Cervical Spine ed 4PhiladelphiaLippincott Williams and Wilkins2004. 746768

  • 6

    Brodbelt ARStoodley MAWatling AJones NR: Cerebrospinal fluid flow in the excitotoxic model of posttraumatic syringomyelia. ANZ J Surg 72:SupplA642002. (Abstract)

  • 7

    Brodbelt ARStoodley MAWatling AMTu JJones NR: Fluid flow in an animal model of post-traumatic syringomyelia. Eur Spine J 12:3003062003

  • 8

    Brugières PIdy-Peretti IIffenecker CParker FJolivet OHurth M: CSF flow measurement in syringomyelia. AJNR Am J Neuroradiol 21:178517922000

  • 9

    Chang HSJoko MMatsuo NKim SDNakagawa H: Subarachnoid pressure-dependent change in syrinx size in a patient with syringomyelia associated with adhesive arachnoiditis. Case report. J Neurosurg Spine 2:2092142005

  • 10

    Fischbein NJDillon WPCobbs CWeinstein PR: The “presyrinx” state: a reversible myelopathic condition that may precede syringomyelia. AJNR Am J Neuroradiol 20:7201999

  • 11

    Ford MDNikolov HNMilner JSLownie SPDeMont EMKalata W: PIV-measured versus CFD-predicted flow dynamics in anatomically realistic cerebral aneurysm models. J Biomech Eng 130:0210152008

  • 12

    Greitz D: Unraveling the riddle of syringomyelia. Neurosurg Rev 29:2512632006

  • 13

    Heiss JDPatronas NDeVroom HLShawker TEnnis RKammerer W: Elucidating the pathophysiology of syringomyelia. J Neurosurg 91:5535621999

  • 14

    Hofmann EWarmuth-Metz MBendszus MSolymosi LPhase-Contrast MR: Imaging of the cervical CSF and spinal cord: volumetric motion analysis in patients with Chiari I malformation. AJNR Am J Neuroradiol 21:1511582000

  • 15

    Klekamp JVolkel KBartels CJSamii M: Disturbances of cerebrospinal fluid flow attributable to arachnoid scarring cause interstitial edema of the cat spinal cord. Neurosurgery 48:1741762001

  • 16

    Levine DN: The pathogenesis of syringomyelia associated with lesions at the foramen magnum: a critical review of existing theories and proposal of a new hypothesis. J Neurol Sci 220:3212004

  • 17

    Levy EIHeiss JDKent MSRiedel CJOldfield EH: Spinal cord swelling preceding syrinx development. J Neurosurg 92:93972000

  • 18

    Lichtor TEgofske PAlperin N: Noncommunicating cysts and cerebrospinal fluid flow dynamics in a patient with a Chiari I malformation and syringomyelia—part I. Spine 30:133513402005

  • 19

    Lichtor TEgofske PAlperin N: Noncommunicating cysts and cerebrospinal fluid flow dynamics in a patient with a Chiari I malformation and syringomyelia—part II. Spine 30:146614722005

  • 20

    Millasseau SCKelly RPRitter JMChowienczyk PJ: Determination of age-related increases in large artery stiffness by digital pulse contour analysis. Clin Sci (Lond) 103:3713772002

  • 21

    Oldfield EHMuraszko KShawker THPatronas NJ: Pathophysiology of syringomyelia associated with Chiari I malformation of the cerebellar tonsils. Implications for diagnosis and treatment. J Neurosurg 80:3151994

  • 22

    Pekkan Kde Zélicourt DGe LSotiropoulos FFrakes DFogel MA: Physics-driven CFD modeling of complex anatomical cardiovascular flows—a TCPC case study. Ann Biomed Eng 33:2843002005

  • 23

    Rennels MLGregory TFBlaumanis ORFujimoto KGrady PA: Evidence for a ‘paravascular’ fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res 326:47631985

  • 24

    Stoodley MAJones NRBrown CJ: Evidence for rapid fluid flow from the subarachnoid space into the spinal cord central canal in the rat. Brain Res 707:1551641996

  • 25

    Williams B: Pathogenesis of post-traumatic syringomyelia. Br J Neurosurg 8:1141151994

  • 26

    Wolpert SMBhadelia RABogdan ARCohen AR: Chiari I malformations: assessment with phase-contrast velocity MR. AJNR Am J Neuroradiol 15:129913081994

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 147 147 18
Full Text Views 224 224 2
PDF Downloads 131 131 2
EPUB Downloads 0 0 0

PubMed

Google Scholar