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A poroelastic fluid–structure interaction model of syringomyelia

Published online by Cambridge University Press:  10 November 2016

Matthias Heil*
Affiliation:
School of Mathematics, University of Manchester, Oxford Road, Manchester M13 9PL, UK
Christopher D. Bertram
Affiliation:
School of Mathematics and Statistics, University of Sydney, NSW 2006, Australia
*
†Email address for correspondence: M.Heil@maths.manchester.ac.uk

Abstract

Syringomyelia is a medical condition in which one or more fluid-filled cavities (syrinxes) form in the spinal cord. The syrinxes often form near locations where the spinal subarachnoid space (SSS; the fluid-filled annular region surrounding the spinal cord) is partially obstructed. Previous studies showed that nonlinear interactions between the pulsatile fluid flow in the SSS and the elastic deformation of the tissues surrounding it can generate a fluid pressure distribution that would tend to drive fluid from the SSS into the syrinx if the tissue separating the two regions was porous. This provides a potential explanation for why a partial occlusion of the SSS can induce the growth of an already existing nearby syrinx. We study this hypothesis by analysing the mass transfer between the SSS and the syrinx, using a poroelastic fluid–structure interaction model of the spinal cord that includes a representation of the partially obstructed SSS, the syrinx and the poroelastic tissues surrounding these fluid-filled cavities. Our numerical simulations show that poroelastic fluid–structure interaction can indeed cause an increase (albeit relatively small) in syrinx volume. We analyse the seepage flows and show that their structure can be captured by an analytical model which explains why the increase in syrinx volume tends to be relatively small.

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Papers
Copyright
© 2016 Cambridge University Press 
Figure 0

Figure 1.Sketch of the axisymmetric model. Cerebrospinal fluid (CSF; cyan) occupies the annular spinal subarachnoid space (SSS) which is partly occluded by a blockage. The syrinx is the fluid-filled cavity inside the spinal cord. In the top figure different colours identify the different tissues; see text for details. The fluid occupying the SSS is subject to an oscillatory pressure at the cranial end of the SSS. Note the large aspect ratio, $L/{\mathcal{D}}=30$, where ${\mathcal{D}}=20~\text{mm}$ is the maximum outer diameter of the SSS (at its cranial end). The dashed line indicates the position of the radial slice across which we compute the volume fluxes that are documented in figure 2.

Figure 1

Figure 2.(a) Time trace of the non-dimensional forcing pressure, $P_{cranial}(t)/\widehat{{\mathcal{P}}}$. (b) The resulting volume flux into the SSS at $z=0$ (black solid); through the narrow gap under the block at $z/{\mathcal{D}}=-7.5$ (blue dashed); through a radial slice across the syrinx at the same axial position (red dash–dotted). The location of the radial slice is indicated by the dashed line in figure 1. Time is non-dimensionalised on the period of the oscillation, ${\mathcal{T}}$. The volume fluxes are scaled on ${\mathcal{U}}{\mathcal{D}}^{2}$ where ${\mathcal{U}}=(\widehat{{\mathcal{P}}}/\unicode[STIX]{x1D70C}_{fluid})^{1/2}$ is the inertial velocity scale. The volume flux is positive when it is directed into the SSS, i.e. away from its cranial end.

Figure 2

Figure 3.Four snapshots of the fluid pressure distribution (colour contours) and the tissue deformation at (a) $t/{\mathcal{T}}=9$, (b) $t/{\mathcal{T}}=9.25$ (c) $t/{\mathcal{T}}=9.5$, (d) $t/{\mathcal{T}}=9.75$. For each snapshot we show the system in its actual 1:1 aspect ratio (bottom) and with the radial dimensions stretched by a factor of 10 (middle and top). In the top panel the tissue displacements are exaggerated by a factor of 20. The pressure is non-dimensionalised on the amplitude of the forcing pressure, $\widehat{P}$.

Figure 3

Figure 4.(a,b) Contour plots of the axial (top) and radial (middle) fluid velocities, and the fluid pressure (bottom) in the SSS in the vicinity of the block, plotted using the actual aspect ratio and the same orientation as in figure 1. (a) $t/{\mathcal{T}}=9.25$, (b) $t/{\mathcal{T}}=9.75$. Bottom: profiles of the axial velocity in radial slices across the deforming SSS, $u_{z}(r,t)$, at (c) $z/{\mathcal{D}}=-7.5$ (in the gap between block and cord), (d) $z/{\mathcal{D}}=-3$ (in the cranial part of the SSS) at eight uniformly spaced instants over the forcing period, starting at $t/{\mathcal{T}}=9$. Velocities are scaled on the inertial velocity scale, ${\mathcal{U}}=(\widehat{{\mathcal{P}}}/\unicode[STIX]{x1D70C}_{fluid})^{1/2}$, and the pressure on the amplitude of the forcing pressure, $\widehat{{\mathcal{P}}}$.

Figure 4

Figure 5.(a–d) Four snapshots of the instantaneous fluid pressure distribution in the SSS (along the FSI interface with the outer boundary of the cord; dashed line ranging over the entire length of the domain) and on the centreline of the syrinx (at $r=0$; dashed line ranging from $z/{\mathcal{D}}=-11$ to $-4$). (a) $t/{\mathcal{T}}=9$, (b) $t/{\mathcal{T}}=9.25$ (c) $t/{\mathcal{T}}=9.5$, (d) $t/{\mathcal{T}}=9.75$. The solid lines in (a)–(d) show the corresponding cycle-averaged pressures. These are shown more clearly in (e) where we also show (using a thick dash–dotted line) the pressure distributions in the corresponding impermeable system. All pressures are non-dimensionalised on the amplitude of forcing pressure, $\widehat{P}$, and the axial coordinate is scaled on the maximum diameter of the dura, ${\mathcal{D}}$.

Figure 5

Figure 6.(a) Evolution of the relative change in syrinx volume, $\unicode[STIX]{x0394}V_{syrinx}(t)/V_{syrinx}(t=0)$ (black dashed line) and its cycle average (blue solid line) for a permeability of $k=10^{-13}~\text{m}^{2}$. (b) Plot of the cycle average (black solid line), the fit to the exponential (4.2) (thick dashed line), and its asymptotic limit (thin dash–dotted line). Time is scaled on the period of the oscillation, ${\mathcal{T}}$.

Figure 6

Figure 7.(a) Evolution of the relative change in syrinx volume, $\unicode[STIX]{x0394}V_{syrinx}(t)/V_{syrinx}(t=0)$ for three different values of the permeability. (b) Plot of the cycle averages (black solid lines), the fits to the exponential (4.2) (thick dashed line) and their asymptotic limits (thin dash–dotted line). $k=10^{-14}\,\text{m}^{2},10^{-13}\,\text{m}^{2},10^{-12}\,\text{m}^{2}$ increasing in the direction of the arrow. Time is scaled on the period of the oscillation, ${\mathcal{T}}$.

Figure 7

Figure 8.(a) Cycle-averaged seepage velocity, $(\overline{\boldsymbol{q}}\boldsymbol{\cdot }\boldsymbol{n})\boldsymbol{n}$, crossing the FSI interfaces between the cord and the SSS (top) and the syrinx (bottom). The FSI interfaces (black lines) have been separated vertically for clarity but are otherwise drawn using the actual aspect ratio. The closed loop indicates the direction of the circular seepage flow. (b) Cycle-averaged normal traction $-\overline{p_{pore}}\boldsymbol{n}$, acting onto the cord. All for $k=10^{-13}~\text{m}^{2}$. The axial coordinate is scaled on the maximum diameter of the dura, ${\mathcal{D}}$.

Figure 8

Figure 9.Profiles of (a) the radial component of the seepage velocity, $q_{r}(r,t)$, (b) the pore pressure, $p_{pore}(r,t)$, in a radial slice through the syrinx cover (at $z/{\mathcal{D}}=-7.5$) at eight uniformly spaced instants over the forcing period, starting at $t/{\mathcal{T}}=9$. The blue solid line shows the results from the full FSI model; the black dashed lines show the predictions from the analytical model discussed in § 4.1, where we approximated the forcing due to the fluid pressure and the axial strain by their first two Fourier components. The seepage velocity is scaled on the inertial velocity scale, ${\mathcal{U}}=(\widehat{{\mathcal{P}}}/\unicode[STIX]{x1D70C}_{fluid})^{1/2}$, the pore pressure on the amplitude of the forcing pressure, $\widehat{{\mathcal{P}}}$ and the radial coordinate on the maximum diameter of the dura, ${\mathcal{D}}$.

Figure 9

Figure 10.Profiles of the radial component of the seepage velocity, $q_{r}(r,t)$, (a,c,e,g), and the pore pressure, $p_{pore}(r,t)$, (b,d,f,h) in a radial slice through an axially uniform model of the syrinx cover at eight uniformly spaced instants over the forcing period. The blue solid line shows the results from the finite element-based solution of the poroelastic equations (2.3)–(2.7), time integrated until a time-periodic steady state was established; the black dashed lines show the predictions for the time-periodic state from the analytical model discussed in § 4.1. (a,b) $k=10^{-13}~\text{m}^{2}$, (c,d) $k=10^{-14}~\text{m}^{2}$, (e–h) $k=10^{-15}~\text{m}^{2}$. In (a–f) we made the syrinx cover uniform by setting $E_{drained}^{[pia]}=E_{drained}^{[cord]}$; in (g,h) we employed the actual stiffnesses, resulting in a much stiffer pia. The seepage velocity is scaled on the inertial velocity scale, ${\mathcal{U}}=(\widehat{{\mathcal{P}}}/\unicode[STIX]{x1D70C}_{fluid})^{1/2}$, the pore pressure on the amplitude of the forcing pressure, $\widehat{{\mathcal{P}}}$, and the radial coordinate on the maximum diameter of the dura, ${\mathcal{D}}$.

Figure 10

Figure 11.Plots illustrating the effect of changing the geometry of the syrinx. (a) and (b) The cycle-averaged seepage velocity and normal traction acting onto the cord (as in figure 8; see caption to that figure for details) when the conical ends of the syrinx in the original model are changed to ellipsoids. (c) Cycle average of the relative change in syrinx volume, $\overline{\unicode[STIX]{x0394}V_{syrinx}}(t)/V_{syrinx}(t=0)$ (red solid line), the fit to the exponential (4.2) (thick dashed line), and its asymptotic limit (thin dash–dotted line) for the two syrinx geometries. Time is scaled on the period of the oscillation, ${\mathcal{T}}$. (d–f) Comparison of the cycle-averaged syrinx deformation for the (d) original and (e) ellipsoidal syrinx shape. Broken lines: undeformed shape; solid lines: deformed shape. (f) Direct comparison between the deformed cycle-averaged syrinx shapes for the two geometries. All displacements are exaggerated by a factor of 40 and lengths are scaled on the maximum diameter of the dura, ${\mathcal{D}}$. $k=10^{-13}~\text{m}^{2}$.

Figure 11

Figure 12.(a) Relative change in syrinx volume (instantaneous and cycle averaged, as in figure 6) for $k=10^{-13}\,\text{m}^{2}$ for syrinxes of different length, increasing in the direction of the arrow. (b) Plot of the four syrinxes (in the $(r,z)$ plane) using a 1:1 aspect ratio.

Figure 12

Figure 13.Relative change in syrinx volume (instantaneous and cycle averaged, as in figure 6) for $k=10^{-13}~\text{m}^{2}$ with (solid) and without (dashed) the inertial terms in (2.3) and (2.4). (b) Relative change in syrinx volume for $k=10^{-12}~\text{m}^{2}$, allowing ($\unicode[STIX]{x1D6FE}^{-1}=\unicode[STIX]{x1D707}_{fluid}^{-1}$; solid) and not allowing ($\unicode[STIX]{x1D6FE}^{-1}=0$; dashed) for tangential slip at the FSI interfaces.

Figure 13

Figure 14.Evolution of the relative change in syrinx volume, $\unicode[STIX]{x0394}V_{syrinx}(t)/V_{syrinx}(t=0)$ for the standard resolution (red solid line); an increased temporal (thick blue dashed line) and spatial (markers) resolution, respectively. Parameters as in figure 6.