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Blood flow in the choriocapillaris

Published online by Cambridge University Press:  02 June 2015

M. A. Zouache*
Affiliation:
Institute of Ophthalmology, University College London, 11-43 Bath Street, London EC1V 9EL, UK
I. Eames
Affiliation:
Department of Mechanical Engineering, University College London, Torrington Place, London WC1E 7JE, UK
P. J. Luthert
Affiliation:
Institute of Ophthalmology, University College London, 11-43 Bath Street, London EC1V 9EL, UK
*
†Email address for correspondence: moussa.zouache.10@ucl.ac.uk

Abstract

The choriocapillaris is a capillary bed located in a thin layer adjacent to the outer retina and is part of the oxygen delivery system to the photoreceptors of the eye. The blood flow is approximately planar and is serviced by microvessels, which join the choriocapillaris through inlets perpendicular to its plane. Capillaries are densely organised and separated by avascular septal posts, which direct the blood flow. The capillary bed is composed of a juxtaposition of tessellating vascular units called lobules, which are filled and drained independently from each other. A theoretical analysis of the blood flow in an idealised model of a lobule of the choriocapillaris is developed and studied. Lobules are modelled as tessellating polygonal prisms, where the upper and lower surfaces correspond to planar parallel membranes. The septae are modelled as cylinders randomly distributed between the two membranes. Feeding arterioles and draining venules are modelled as inlets and outlets connecting at the lower surface of the prism perpendicularly to the plane of the lobule. An inlet is placed inside the lobule, while an outlet is placed at each of the vertices. The polygonal prism can be formally subdivided into a set of triangular prisms with one inlet and two outlets, each of them located at one of the vertices. The triangular prisms are taken to be isosceles, and are therefore characterised by a vertex angle ${\it\omega}$ at the inlet and a span $L$ . The flow is viscously dominated, and is investigated in the lubrication limit, in which the characteristic thickness of the prism is much smaller than the diameter of the cylinders. As a result of the geometry, a stagnation point is located midway between the outlets. A separation streamline joins the inlet and the stagnation point. The pressure drop ${\rm\Delta}\tilde{p}$ and the average fluid particle residence time $\langle \tilde{T}\rangle$ are analysed as a function of the angle at the inlet ${\it\omega}$ and the septae volume fraction ${\it\Phi}$ . When no cylinders are present ( ${\it\Phi}=0$ ), an analytical expression for the pressure field is calculated by conformal mapping. Close to the triangle walls, the flow is quasi-parallel and characterised by a shorter fluid particle residence time. In the vicinity of the stagnation point, the velocity decreases and the residence time diverges logarithmically with the distance to the stagnation streamline. The minimum in pressure drop corresponds to a maximum in residence time, and is obtained for ${\it\omega}={\rm\pi}/2$ . Asymptotic expressions for the pressure drop and average residence time are formulated in both the limits $\Vert {\it\omega}\Vert \ll 1$ and $\Vert {\rm\pi}-{\it\omega}\Vert \ll 1$ . The impact of ${\it\Phi}$ on the flow is characterised by solving the equations for the flow numerically and using the Darwin drift framework. We show that the pressure drop is approximately proportional to $1+2{\it\Phi}$ for relatively small ${\it\Phi}$ , and that $\langle \tilde{T}\rangle$ is proportional to $1-{\it\Phi}$ regardless of the void fraction or shape of the septae. In the case ${\it\Phi}=0$ , the average residence time equals the volume of the domain divided by the volumetric flux. This analysis provides a new perspective on the blood flow dynamics within the choriocapillaris. Lobules form systems, where perfusion and corpuscle transport are a function of the angle that any two venular openings make with an arteriolar opening, the surface area perfused and the void volume fraction. The blood flow velocity and residence time are significantly heterogeneous, which may be responsible for the high degree of selective localisation observed in the pathogenesis of some inflammatory and degenerative diseases of the eye.

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Papers
Copyright
© 2015 Cambridge University Press 
Figure 0

Figure 1. Diagram of a human eye (a) and schematic of the cellular arrangement of the choroid and retina (b) within the rectangular element highlighted in (a). Incident light is directed and scattered towards the back of the eye by the cornea, iris and lens. Photons are then converted into electro-chemical impulses sent to the brain by the photoreceptors, which are supplied in metabolites by the choroidal vasculature lying underneath the retina (b). Portions of human choroid were immunostained for blood vessel markers and imaged at different depths (c,d). The choriocapillaris, seen from the retinal side in (c), is composed of tightly organised capillaries separated by septae (arrow), which direct the blood flow. The underlying vessels from the outer choroid (d) travel parallel to the plane of the choriocapillaris, branch extensively, and ultimately insert into the choriocapillaris perpendicularly to its plane. Image (d) corresponds to a plane underneath the capillaries (some of which are still visible). Round openings can be observed at the connection between the vessels from the outer choroid and the capillaries (arrows).

Figure 1

Figure 2. Fluorescein angiogram of the choriocapillaris, taken with permission from Hayreh (1974b) (the scale bars are missing from the original publication). The fluorescent dye injected in the general circulation begins to appear in the choriocapillaris in (a), revealing the lobular organisation. Each lobule is filled through the arteriolar opening located at its centre. The number of lobules illuminated is maximal a few seconds later, as shown in (b), where the boundary between lobules has been added as a series of connected black lines. The dye is then evacuated through the periphery of the lobules, as shown in (c).

Figure 2

Table 1. List of physiological parameters characterising the geometry and fluid properties of a choriocapillaris lobule. When a range of values is given, the value used is marked with an asterisk. The flow rate at the arteriole was estimated from the average capillary blood velocity and the radius of the inlets. The vertex angle was approximated from angiography images.

Figure 3

Figure 3. The flow is studied in an isosceles triangle ${\it\Omega}$ characterised by a vertex angle ${\it\omega}$ and a side length $L$. One inlet and two outlets are placed at its vertices. The choriocapillaris septae are modelled by cylinders of constant diameter $2a$ randomly distributed over the triangle. A prescribed area flux into the triangular domain $q$ is imposed at the inlet. A zero-pressure boundary condition is imposed at the outlets.

Figure 4

Figure 4. The Schwarz–Christoffel conformal map is calculated to transform the triangular domain in (a) into the half-plane in (b). In (b), the source of strength $k$, sinks of strength $-k/2$ and representative streamlines are shown. (a) Real plane (${\it\omega}$), (b) transformed plane (D).

Figure 5

Figure 5. Streamlines of the flow (a,b), pressure field (c,d) and instant velocity profile (e,f) calculated using the conformal mapping solution for ${\it\omega}={\rm\pi}/2$ and ${\it\omega}={\rm\pi}/4$ respectively. The instant velocity was plotted over a reduced range of values.

Figure 6

Figure 6. Evolution of (a) the residence time as a function of the normalised angle at the inlet $\tilde{{\it\theta}}$, (b) the c.d.f. and (c) the complementary c.d.f. calculated using the conformal mapping solution for increasing values of ${\it\omega}$; (c) is plotted on a semi-logarithmic scale ($y$ axis).

Figure 7

Figure 7. Sketch of the system of coordinates used for the asymptotic analysis of the residence time close to the stagnation point (a) and semi-logarithmic plot of the residence time as a function of the angle at the inlet (b) for ${\it\alpha}={\rm\pi}/3$. As ${\it\theta}\rightarrow 0$ the residence time diverges logarithmically.

Figure 8

Figure 8. Evolution of (a) the pressure drop and (b) the residence time and root of the mean square of the residence time (dash-dotted line) with the angle at the inlet ${\it\omega}$ calculated analytically by conformal mapping (solid line) and numerically using the FEM method ($+$). The asymptotic expressions (3.32)–(3.34) are plotted as dashed lines. The minimum value of the pressure drop and the maximal value for the average residence time are obtained for ${\it\omega}={\rm\pi}/2$.

Figure 9

Figure 9. (a) Definition sketch of the drift volume in a diverging channel and (b) evolution of the residence time as a function of $x/W_{i}$ for decreasing values of $W_{i}$. In (a), the dashed line corresponds to the flow profile in the absence of the cylinder. In (b), the dashed line corresponds to the residence time for the geometry described in (a) in the absence of the cylinder.

Figure 10

Figure 10. Streamlines of the flow (a,b), pressure field (c,d), residence time distribution (e) and c.d.f. ( f) for ${\it\omega}={\rm\pi}/3$, ${\it\Phi}=0.13$ and ${\it\Phi}=0.3251$. The residence time and c.d.f. for ${\it\Phi}=0$ and ${\it\Phi}=0.0332$ are also shown. The residence time was calculated for 1000 particles released at the inlet.

Figure 11

Figure 11. Streamlines of the flow (a,b), pressure field (c,d), residence time distribution (e) and c.d.f. (f) for (${\it\omega}={\rm\pi}/2$, ${\it\Phi}=0.2881$) and (${\it\omega}={\rm\pi}/4$, ${\it\Phi}=0.2853$). The dotted lines correspond to ${\rm\Delta}\tilde{T}$ and the c.d.f. when ${\it\Phi}=0$. The residence time was calculated for 1000 particles released at the inlet.

Figure 12

Figure 12. Evolution of (a) the pressure drop ${\rm\Delta}\tilde{p}/{\rm\Delta}\tilde{p}({\it\Phi}=0)$ and (b) the residence time $\langle \tilde{T}\rangle /\langle \tilde{T}\rangle ({\it\Phi}=0)$ (calculated for 400 particles released at the inlet) with the void volume fraction ${\it\Phi}$ for a fixed distribution of cylinders for a range of ${\it\omega}$. The approximate and analytical expressions obtained for ${\rm\Delta}\tilde{p}$ and $\langle \tilde{T}\rangle$ are plotted as dashed lines. The arrow under ‘Physiological range’ appears to be thicker in (a) than it is in (b).