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Transcript
The concept of end arteries and diversion
of blood flow
Chester Hyman
Examination of the circulation in peripheral tissues has established the validity of certain
theoretical hemodynamic concepts. The redistribution of blood flow between parallel vascular
beds during unequal changes in their resistances seems to obey the general predictions of
simple diversion. Such shifts of blood between vascular systems are exaggerated when the
local perfusion pressure is diminished by abnormal upstream resistance. Diversion, as well as
the deleterious effects of arterial occlusion, can be minimized if an adequate collateral circulation is established soon enough to prevent damage to the ischemic tissue. For tissues supplied
by a true end artery, such collateral supply is ruled out by definition. Within the orbit the
retinal artery is in fact an end artery while the ophthalmic artery may receive certain small
collaterals. Redistribution of blood between the retina and the other orbital tissues is at least
theoretically possible, and evidence for such a diversion should be sought in cases with clearly
established partial occlusion of the ophthalmic artery. Since the retinal artery supplies only
a single tissue, the diversions are limited to those betweeen the various portions of the retina,
or between a nutritive or shunt circulation. Evidence for the latter type of diversion has already
been presented. We suggest that it might be of value to check these theoretical projections
by direct experimentation insofar as possible; findings of such studies should assist us in describing the dynamics of intraorbital blood flows.
D,
remain constant, dilatation of any of the
routes for runoff lowers the pressure at the
arterial end of the parallel undilated beds
and thus diminishes their perfusion. The
pressure drop depends on the magnitude
of the dilatation in the distal bed, but it
is also influenced by the resistance central
to the point.2 Normally, the resistance in
the proximal arteries is insignificant; the
major pressure drop occurs across the distal
resistances, and dilatation of a peripheral
bed has a minimal effect on the local arterial pressure. However, in pathologic
conditions where resistance proximal to
the branching constitutes a considerable
fraction of the total resistance, increasing
runoff lowers pressure to levels below the
limits for which tissues can compensate.3
Only if a relatively unaltered pressure at
the choice point can be assured, can blood
flow in the undilated pathways be main-
iversion of blood flow to a dilated system of blood vessels at the expense of an
undilated parallel system is most obvious
where the pressure in the artery proximal
to the bifurcation is significantly lowered.1
Normally the artery supplies sufficient
blood flow to maintain adequate local pressure in the face of maximum tissue needs,
i.e., when resistance falls to minimal levels.
The pressure at any point in a peripheral
artery is determined by three factors: central arterial pressure, resistance in the
vessels upstream from the point under consideration, and total runoff through the
distal branches. Thus, if all other factors
From the Department of Physiology, University
of Southern California School of Medicine, Los
Angeles, Calif.
Supported by United States Public Health Service
Grant HE-00352-15.
1000
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Volume 4
Number 6
tained. When a major artery is occluded or
narrowed, restoration of pressure depends
on the supply of more blood to the system
distal to the occlusion via adequate collaterals.4
How existing or potential collateral circulation modifies local arterial pressure and
hence diversion is a function of the relative amounts of flow through the original
arterial supply and the new collateral system suggested by Fig. 1. The arrangements
of alternative arterial pathways are morphologically varied.5 For example, the
circle of Willis or the arches in the distal
portions of the extremities, as in Fig. 2,a,
unite several major arteries into a single
system which then furnishes the blood to
the tissues beyond. Frequently, only one of
the arteries feeding the common path may
suffice to satisfy the needs of the tissues
beyond. In other situations only a potential
alternative collateral pathway is present,
i.e., small parallel arteries which ordinarily
carry only a small fraction of the total
blood to the tissue, but which dilate to
provide an adequate collateral supply
after occlusion of the major vessel. The
mechanisms involved in opening of these
vessels is still uncertain0: Modification of
the pressure gradient resulting from the
drop in the distal portion of the original
major artery must play some role,7 but
Fig. 1. Role of collaterals in restoring pressure to
an artery beyond a point of partial occlusion.
Unless there is a collateral supply, indicated by
the dotted line, dilatation of one system beyond
the point of occlusion would decrease the pressure
at the point of bifurcation. This would then lead
to an inadequate perfusion of the cognate, undilated bed.
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End arteries and blood flow diversion 1001
other factors (chemical8 or nervous9) may
intervene. Another type of collateral circulation carries blood around the occlusion
through very small branches which connect
with terminal portions of some other vascular trees. Because the hemodynamic resistance is quite high, blood flow through
such pathways will be limited unless they
are numerous, or the occlusion is at a point
where the original resistance to the point
of anastomosis was almost as great. Finally,
in certain tissues true end arteries may
exist, i.e., unique paths with neither real
nor potential alternatives to supply the
tissues (Fig. 2,b). Whether or not morphologically demonstrable end arteries exist
in the body is still uncertain; the smaller
coronary arterial branches have at times
been considered as essential for supplying
myocardial portions, but the conflicting
data in this area leave the question again
unresolved.10
The major blood supply to the orbit is
through the single ophthalmic artery, the
only major vessel entering through the
foramen.11 Although some alternative pathways to this area are morphologically demonstrable, i.e., the ethmoidal vessels,
from the internal carotid, and connections
with the external carotid system might
occur in the periorbital regions, there is
still no evidence that such collaterals can
satisfy the needs of all intraorbital tissues
after occlusion or thrombosis of the ophthalmic artery.11
Obviously the concept of an end artery
carries with it a description of the tissues
which depend on that artery for their
supply. Thus, as suggested by Fig. 3, the
ophthalmic artery is an end artery with
respect to the entire orbital contents,
whereas the retinal artery is an end artery
only for the retina. The practical significance of the collateral circulation is
ultimately determined by the ability of the
tissue to tolerate prolonged ischemia. To
compensate for occlusion of the retinal
artery, an adequate collateral circulation
must manifest itself immediately, for only
a few hours of complete ischemia of the
1002 Hyman
Investigative Ophthalmology
December 1965
Fig. 2. a, arterial supply to the hand with branchings and intercommunications that assure
an adequate, preformed, collateral circulation, b, an end arterial system with no possibility
for alternative supply of blood to any of the arterial branches.
Fig. 3. Schema of circulation to the orbit. Note
that the ophthalmic artery is the sole vessel moving through the foramen. Evidence from several
different sources suggests that blood may enter
the orbit through branches of the maxillary and
mandibular arteries of the external carotid. These
would serve as a collateral supply to the ophthalmic artery system. There is no collateral system
for the retinal artery. Thus, the retinal artery at
point ( J ) is a true end artery for all of the retinal
tissues; whereas the ophthalmic artery (2), except
for the contributions referred to above, is an end
artery for the intraorbital tissues considered as a
whole.
retina suffice to induce irreversible changes;
restoration of flow by collateral circulation
after this time cannot restore function in
any oxygen-dependent tissue.12'13
Diversion of blood among the several
beds supplied by a single vessel is most
obvious if these tissues have vastly differing blood flow demands, and if the need
in one of the tissues varies widely from
time to time. Limiting the arterial supply
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to a relatively uniform group of tissues with
constant blood flow demands would tend
to lower flow uniformly through all of the
distal vascular beds.
Because of inadequate collaterals, partial
occlusion at the point where the ophthalmic
artery passes through the optic foramen
would profoundly diminish the pressure
in all the arteries within the orbit and increase the likelihood of diversions between
the separate tissues. Branches of the ophthalmic artery supply even more varied
tissues than those supplied by the brachiaJ
or the femoral arteries. The retina, with
its high metabolic demands, calls for a very
large blood flow per unit of tissue, but it
is not clear whether this flow varies with
activity. Resting extraocular muscles probably require less flow per unit of tissue
than does the retina, but if such muscles
are similar to skeletal muscle elsewhere,
demand for blood should increase remarkably during and after contraction.14 The
adipose pads and connective tissues within
the orbit are very likely areas of relatively
fixed flow. Finally, the ciliary body and
other secreting organs may require variable
amounts of blood flow. It follows that
lowering pressure in the ophthalmic artery
might seriously deplete blood supply to
those tissues with the highest resistance
and that intermittent vasodilatation in muscles during activity, for example, could
Volume 4
Number 6
induce a corresponding intermittent ischemia of the "undilated" tissues. "Grayout"
might accompany prolonged vigorous eye
movements. In contrast, partial occlusion
of the retinal artery could not significantly
affect the diversion of blood flow between
the retina and the extraocular muscles.
Because it supplies a single tissue, partial
occlusion of the retinal artery would uniformly diminish the flow through the retina.
It might, however, divert the flow among
various retinal regions if their resistances
varied independently, or divert the flow
between nutritional and shunt paths.
Besides diversion between tissues, blood
flow may be shifted from the nutritional
to the nonnutritional, or shunt, vessels.
Thus, even when the total blood supply
to a tissue is constant, shunt vessels can
trade resistance with the parallel nutritional beds to vary the effective circulation.15 It has recently been suggested that
a similar shift to the shunt circulation in
the retina may deplete adjacent nutritional capillary circulation in diabetes.10 It
is interesting to note that Barany17 reached
the same conclusion about a shift to shunt
circulation at the expense of nutrition to
skin in diabetics. Perhaps because of the
fact that the point of increased vascular
resistance in diabetes is in small vessels
beyond the point of entry of significant
collaterals, the situation for diversion between the categories of vessels within the
microcirculation is exaggerated in this
disease.
Dilatation of resistance vessels under
conditions of relative ischemia can compensate in part for the diversion. In skeletal muscle and skin, reactive hyperemia
may lower the resistances to less than a
tenth of normal, which implies the ability
to maintain a constant perfusion in spite
of significantly lowered arterial pressure.
This system for self-regulation of tissue
nutrition has been fairly well documented
in several peripheral systems.18'19 This potential for dilatation of a blood vessel by
the local products of ischemia probably
varies from tissue to tissue, so that extrap-
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End arteries and blood floiu diversion
1003
olation to tissues within the globe is
dangerous.
REFERENCES
1. Hyman, C , and Winsor, T.: Blood flow redistribution in the human extremity, Am. J.
Cardiol. 4: 566, 1959.
2. Winsor, T., and Hyman, C.: Primer of peripheral vascular diseases, Philadelphia, Lea &
Febiger. In press.
3. Hyman, C , and Winsor, T.: Series vascular
resistances, Am. Heart J. 66: 840, 1963.
4. Green, H. D., Cosby, R. S., and Radzow, K.
H.: Dynamics of collateral circulation, Am.
J. Physiol. 140: 726, 1944.
5. Quiring, D. P.: Collateral circulation, Philadelphia, 1949, Lea & Febiger.
6. Liebow, A. A.: Situations which lead to
changes in vascular patterns, in Handbook of
Physiology, Sec. 2, Circulation, vol. 2, 1963,
p. 1251. '
7. John, H. T., and Warren, R.: The stimulus
to collateral circulation, Surgery 49: 14, 1961.
8. Lewis, T.: The adjustment of blood flow to
the affected limb in arterio-venous fistulas,
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9. White, A. E., Flasher, J., and Drury, D. R.:
The effect of lumbar sympathectomy on tine
collateral arterial circulation, Surgery 37:
567, 1955.
10. Wiggers, C. J.: The functional importance of
coronary collaterals, Circulation 5: 609, 1952.
11. Hayreh, S. S.: Arteries of the orbit in the
human being, Brit. J. Surg. 50: 938, 1963.
12. Kornzweig, A. L., Eliasoph, I., and Feldstein,
M.: Occlusive disease of retinal vasculature,
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13. Bossi, R., and Pisani, C : Collateral cerebral
circulation through the ophthalmic artery
and its efficiency in internal carotid occlusion,
Brit. J. Radiol. 28: 462, 1955.
14. Hilton, S. M.: Experiments on the postcontraction hyperemia of skeletal muscle, J.
Physiol. 120: 230, 1953.
15. Ballard, K., Fielding, P., and Hyman, C :
Evidence for the shift of blood to the nutritive circulation during reactive hyperaemia,
J. Physiol. 173: 178, 1964.
16. Cogan, D. C , and Kuwahara, T.: Capillary
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17. Barany, F. R.: Abnormal vascular reactions
in diabetes mellitus, Acta med. scand. Supp.
304, 152: 1, 1955.
18. Hyman, C , Paldino, R. L., and Zimmermann,
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muscle, Circulation Res. 12: 176, 1963.
19. Johnson, P. C : Review of previous studies
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