OUTFLOW
V
The Choroidal Circulation
In contrast to the retinal vessels which are readily
observed through the ophthalmoscope and with the slit lamp,
the arteries and veins of the choroid are concealed behind
the retinal pigment epithelium, and our knowledge of the
choroid is derived largely from laboratory investigation.
Nonetheless there are a few observations that we may make
ourselves. With the ophthalmoscope we see coursing
anteriorly along the temporal and nasal meridian of the eye
the long posterior ciliary arteries each accompanied by a
long posterior ciliary nerve. The choroidal veins are
outlined in broad silhouettes as they converge in stellate
or perhaps pinwheel configuration onto the outflow channel,
hence the name "vortex". The ocular pulse, which is thought
to be caused by the choroid, is reflected in the
"spontaneous" pulsation of the retinal veins on the disc
that we discussed in previous issues of the Glaucoma Letter,
and in the oscillating intraocular pressure that is so
easily demonstrated with tonometry or tonography. At the
time of retinal detachment surgery the emissary channels
from the vortex veins are readily identified on the surface
of the sclera. One searches for them then to protect them
from accidental injury. In eyes with atrophic retinal
pigment epithelium the large vessels of the choroid are
clearly visible. In that situation one may study individual
vessels with contact lens and slit lamp. However, where the
choroid is seen distinctly, the retina must be atrophic.
The same insult that injured the retina is likely to have
damaged also the choroid; and even if this were not the
case, it is likely that atrophy of the retina itself would
induce changes in the overlying tissue. We have no
opportunity, therefore to observe the intact choroidal
circulation directly.
Blood from the choroidal capillaries drains into the
vortex veins and these pass through the sclera to empty into
branches of the ophthalmic vein. From its location inside
the scleral envelope, we infer that the entire intra-ocular
choroidal circulation is potentially subject to the
intraocular pressure. We know also, that on the outside of
the globe, the pressure in the ophthalmic vein into which
the vortex circulation drains is relatively much lower than
the intravascular pressure of the choriocapillaris. As in
the case of the retinal circulation, we infer the existence
of a pressure gradient. But while we can directly observe
the collapse of the veins on the disc that accounts for the
pressure gradient in the retinal venous drainage, the
location of the pressure gradient of choroidal outflow is
not immediately apparent.
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The retinal vein leaves the globe in a direction
perpendicular to the scleral surface, The vortex veins, on
the other hand, take an oblique course through the sclera.
This anatomic configuration has led to the theory that with
increasing intraocular pressure there is progressive
compression of the vortex veins, producing an increased
resistance to flow and thereby preventing the pressure-
induced collapse of the choriocapillaris. Intrascleral
pressure on these obliquely coursing veins was thought to
create the necessary resistance to prevent the emptying of
the choroidal vascular bed. It is an elementary postulate
of physics that the degree to which the vortex vein coursing
through the sclera will be compressed by any given
intraocular pressure is a function of the fluid pressure
within the vein, of the orientation of the vein, of the
depth at which the vein is located within the sclera, and of
the elastic properties of the sclera.
An analogous situation obtains with respect to the
collector channels from the Canal of Schlemm that traverse
the sclera to drain into the aqueous veins. From time to
time the question is raised whether compression of these
vessels might not account for at least part of the
resistance to aqueous outflow. This problem has recently
been in investigated by John L. Battaglioli at the
Massachusetts Institute of Technology in a thesis, "The Role
of Vessel Collapse on the Flow of Aqueous Humor," published
in June 1981. Although Battaglioli studied outflow
resistance from the Canal of Schlemm, his results are
directly applicable to the dynamics of vortex vein drainage,
provided one admits the plausible assumption that there is
no great difference in the elastic moduli of the sclera of
the posterior pole from the elastic moduli of the sclera
adjacent to the limbus.
One can readily visualize that with an increase in
intraocular pressure the sclera stretches. The amount of
stretching for any given increase in pressure is governed by
the tensile modulus of the sclera. As the sclera stretches,
it also becomes thinner. This thinning is considered
identical with the compression which might occur if, for
instance, the sclera were compressed between two rigid
plates. The amount of thinning for any given increase in
pressure is governed by a physical characteristic of the
sclera which is called its compressive modulus. Battaglioli
found that although a number of measurements of the tensile
modulus of sclera have been published, its compressive
modulus was unknown. He built a small hydraulic press with
which he measured the compressive modulus of elasticity of
the sclera. Using this instrumentation Battaglioli found
the compressive modulus to be 3.3 x 10 dynes/cm compared
with a tensile modulus of 3.3 x 10 dynes/cm . These figures
indicate that it requires one hundred times as much force to
stretch as to compress the sclera by a given fraction, a
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ratio which on first thought is surprising, but then, on
second thought seems not incompatible with the clinical
experience of those of us who have had occasion to dissect
and suture sclera in the operating room.
To estimate the magnitude of the stresses induced in
the sclera by the intraocular pressure, Battaglioli relied
on equations published in 1934 by Timoshenko. (S.P.
Timoshenko and J.N. Goodier, "Theory of Elasticity", N.Y.,
1934) For an eye 24 mm in diameter, the tangential stress
ranges from 5.5 times the intraocular pressure at the inner
surface of the sclera to 5 times the intraocular pressure at
the outer surface. The radial stress, on the other hand,
ranges from a value equal to the intraocular pressure on the
inner surface to zero at the outer surface, this last
calculation coinciding nicely with untrained intuition.
Battaglioli then made a mathematical analysis of the
forces governing the behavior of a vessel coursing
tangentially in the sclera. He determined that the
deformation of the vessel within the sclera could be
expressed in terms of seven parameters: tangential stress,
radial stress, tangential modulus, compressive modulus,
Poisson's ratio, pressure within the vessel, and its
undeformed cross-section. These parameters he then grouped
into four dimensionless ratios that could be matched with a
large scale experimental model in all respects except one.
He was unable to find a substance with the same disparity
between compressive and tensile moduli as sclera. He
compromised by using a closed cell foam made of vinyl
chloride rubber, which resembled the sclera in that the
ratio of its tensile modulus to its compressive modulus was
much greater than 1. For the foam, this ratio was 22.5; for
the sclera, as mentioned earlier, it is 100. He then
fashioned an 8" x 8" x 12" rectangular block of the foam and
drilled a 3/8" diameter hole at right angles to the 8" x 8"
surface. Into the hole was inserted a thin plastic tube
filled with electrically conductive fluid, making it
possible at one and the same time to control the pressure
within the simulated vein and to measure its cross-section.
Forces were applied to the foam through rigid plates glued
to its surfaces. Thus it was possible to study how external
pressures on the foam would change the shape of the tube
that passed through it. When the externally applied forces
were scaled to correspond to the calculated stresses that
various intraocular pressures would induce in the sclera, it
became possible to make inferences concerning their effect
on trans-scleral outflow channels.
With this experimental set-up, Battaglioli was able to
show that for a tangentially oriented vessel, depending on
its length and location, scaled pressures of 35 to 55 mm Hg
would be required before the induced scleral deformation led
to a significant pressure drop. For vessels that course not
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tangentially but obliquely, the external pressure required
to collapse the tube becomes much higher. If the vessel
traverses the sclera in a direction radial to the globe,
then increasing the intraocular pressure will cause the
vessel not to collapse, but to dilate.
Battaglioli was concerned with the dynamics of aqueous
outflow. He concluded that resistance in the collector
channels did not contribute to the total outflow resistance
of the eye except possibly at pathologically elevated
pressures. His results, however, are immediately applicable
to the question of whether there may be a pressure drop in
the vortex veins as they traverse the sclera. Battaglioli's
findings strongly suggest that this is not the case, and
that under physiologic conditions, the scleral tunnel is not
the locus of resistance to vortex vein outflow.
Battaglioli's thesis suggests that it may be worthwhile
to take another look at the choroidal circulation, obscured
though it is by the pigment epithelial barrier. When one
looks at the fundus with the ophthalmoscope or with the slit
lamp and the contact lens, one sees broad bands of choroidal
vein like the curved spokes of a wheel converging onto the
exit foramen. On first thought one accepts the profile of
these vessels as indicative of a large volume, consistent
with the well understood vascularity of the choroid. Yet
the observation that in the case of the retina, broad venous
profiles represent not engorged but partially collapsed
vessels, raises the question whether or not the breadth of
the choroidal veins might not reflect partial collapse
rather than engorgement. This suspicion appears to be
confirmed in the occasional situation when, because of
atrophy of the retinal pigment epithelium one has an
opportunity to study choroidal veins stereoscopically with
the slit lamp. One sees then that at least some, and
perhaps most of the choroidal veins whose contours are
visible with the ophthalmoscope far from being cylindrical,
are actually flat ribbons. Only occasionally does one see a
choroidal vein that is even partially distended.
Fluorescein angiography of areas in the fundus that have
been denuded of pigment epithelium shows that the choroid's
broad veins often fill with only a thin layer of blood.
It follows that unlike the healthy retinal venous
vascular bed whose volume remains practically unaffected by
changes in the intraocular pressure, the volume of the
choroidal venous vasculature is unstable. The collapse of a
choroidal vein implies that its contents have been partially
expressed, and the volume of the choroidal venous plexus
therefore may be expected to vary inversely with the
intraocular pressure. The fluctuation of choroidal volume
with intraocular pressure will be reflected in fluctuating
meridional stresses of the choriocapillaris and of Bruch's
membrane as spherical shells. When the intraocular pressure
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decreases, the volume of blood in the choroidal veins
increases, the inner layers of the choroid are displaced
centrally, and the stress induced in them by the intraocular
pressure diminishes. On the other hand, if the intraocular
pressure increases, then the choroid flattens, and Bruch's
membrane, displaced toward the periphery of the globe,
becomes correspondingly stretched. This tension in the
choroid is transmitted to the ciliary body to which the
choroid is anchored, and through it to the scleral spur.
With an increase in intraocular pressure then, the choroid
tends to collapse, its inner layers are pushed outward by
the intraocular pressure, there is increased meridional
stress which makes posterior traction on the scleral spur,
and which, analogous to the effect of a miotic, will tend to
open the canal of Schlemm and restore the intraocular
pressure to a more normal level. It is unknown what role,
if any, this mechanism might have in the control of the
intraocular pressure.
There is a second corollary to these considerations.
Just as the collapsed segments of retinal vein provide a low
pressure drainage system to the temporal and nasal portions
of the disc, so the collapsed segments of choroidal vessel
offer a low pressure sink for those venules and capillaries
of the choroid that drain into them. We do not have
sufficient anatomic or physiologic data to draw conclusions
about the extent of this drainage, but it may constitute a
substantial proportion of the choroidal circulation. In any
event, the low pressure choroidal veins and such capillary
tributaries as they may have constitute potentially a second
outflow system for aqueous. It is held that as much as 20%
of the aqueous drains from the anterior chamber angle into
the ciliary body and choroid, whence it is eliminated from
the eye by mechanisms unknown. The classical postulate that
the site of choroidal outflow resistance is the compressed
vortex vein within the sclera entails the inference that the
entirety of the choroidal circulation within the globe
should be above intraocular pressure. Aqueous, therefore,
if it were to enter the choroidal circulation, could do so
only by negotiating a pressure gradient. Thus one should
also have to postulate the existence of an osmotic or of an
active transport mechanism to convey aqueous into the
choroidal capillaries, or alternatively one should have to
assume some anatomically obscure extravascular pathway by
which the uveo-scleral flow might escape from the globe,
avoiding the choroidal capillaries and veins. The presence
within the choroid of a network of collapsed vessels whose
contents are under less than intraocular pressure may help
to explain how aqueous leaves the eye by the uveo-scleral
route.
The existence of such an intraocular network of
collapsed vessels in the outflow segment of the choroidal
circulation may also shed some light on that troublesome
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pathophysiologic phenomenon, the choroidal effusion. It is
likely that the accumulation of fluid in the suprachoroidal
space in many instances reflects the diminution or loss of
the gradient between the intraocular pressure and the
pressure in the choroidal veins. Choroidal effusions are
seen most commonly after filtering surgery, when the
intraocular pressure has been purposely reduced. In that
situation the absence of significant intraocular pressure
prevents the expression of blood from the choroidal veins
through the vortex veins into the extraocular venous bed.
The choroidal veins then become distended with blood under
pressure from the capillaries. That portion of the
capillary circulation which normally drains into the
collapsed low pressure veins must now flow into veins whose
contents are under significantly higher tension. The
resultant stasis, whether from failure of reabsorption or
from abnormal transudation, may well explain the consequent
choroidal effusion.
Choroidal effusions are also observed when the pressure
in the ophthalmic vein is elevated, as occurs, for example,
in Sturge-Weber disease or with dural shunts. If outflow
resistance in the choroidal circulation were the result of
pressure induced scleral stresses, these elevations of
ophthalmic venous pressure would be ineffective in raising
intraocular venous pressure, and for this reason: Stress of
the sclera is a function of the difference between
intraocular and extraocular pressures. Increasing the
extraocular pressure is just as effective as lowering the
intraocular pressure in reducing that stress. An increase
in ophthalmic venous pressure results in an increase in the
interstitial pressure of the orbital tissues, i.e., an
increase in extraocular pressure. The increased extraocular
pressure brings about a corresponding decrease in scleral
stress, and hence a decrease in the resistance to flow
within the sclera. If the choroidal venous pressure rises
nonetheless, this is the case because the elevated
ophthalmic venous pressure is transmitted directly to the
vortex veins within the globe, and we may assume that it
causes congestion, transudation and edema there much as
occurs at the optic disc in the presence of elevated
intracranial pressure. A disruption of the vortex vein, as
at retinal surgery, causes stasis and effusion by a similar
mechanism.
Finally, if intraocular pressure is markedly elevated,
as occurs at times after retinal surgery, where placement of
an encircling band suddenly raises the tension, then, as
predicted by Battaglioli, pressures may indeed rise high
enough to compress the vortex vein in its scleral tunnel and
thereby to obstruct venous drainage with ensuing choroidal
detachment. It is also possible that scleral compression
with secondary engorgement of the ciliary body and or
choroidal effusion contributes to the anterior displacement
of the lens-iris diaphragm in the angle closure glaucomas,
especially those that occur in the presence of patent
iridectomies and in the absence, therefore, of pupillary
block.
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