Exp. Eye Res. (1995) 61, 699-711
AlteredVasoactivity in the Early Diabetic Eye' Measured in the
Isolated Perfused Rat Eye
ER-NINGSU, DAO-YI YU, VALERIEA. ALDER*, PAULA K. YUAND STEPHEN J. CRINGLE
Centre for Ophthalmology and Visual Science, Lions Eye Institute, University of Western Australia,
Ned/ands WA 6009, Australia
(Received Lund 25 January 1995 and accepted in revised form 26 July 1995)
The effect of 4 weeks streptozotocin-induced diabetes on ocular vascular resistance responses to
noradrenalin (NA), adrenalin (A), phenylephrine (PHE), isoproterenol (ISOP), prostaglandin F2~(PGF2:).
5-hydroxytryptamine (5-HT) and angiotensin II (ANG II), was determined using a newly-developed,
isolated, arterially-perfused rat eye preparation, by comparing responses from control and diabetic eyes.
After extensive preliminary experiments to establish optimum parameters, the ophthahnic artery of
enucleated control and diabetic rat eyes was cannulated and the retinal and uveal vasculature perfused
at a constant flow with Na+-Krebs solution after streptozotocin-induced diabetes had been established for
4 weeks. The eyes were maintained in an environment-controlled organ bath. Perfusion pressure was
monitored as increasing log M concentrations of agonists were added to the perfusate. Total ocular
resistance could be calculated from knowledge of flow and pressure.
In control eyes, NA, A, PHE, PGF2~, and 5-HT all produced dose-dependent increases in total vascular
resistance, with the following order of potency: NA = A > 5-HT > PHE = PGF2~ at 10 4 M. The ocular
circulation was not sensitive to isoproterenol and angiotensin II. In diabetic eyes responses to NA, A.
PGF.2~and 5-HT were altered. Diabetic responses to NA and A had lower thresholds with larger resistance
increases at low concentrations. However, the rate of increase in resistance with concentration was more
gradual in diabetic eyes so that at lO-4M control responses were larger. Diabetic resistance responses to
PGF2~ had the same threshold as in control eyes, but were greater in magnitude with an earlier peak at
10 -4 M. In contrast diabetic resistance responses to 5-HT were reduced, peaked at a lower resistance
at 10 4 M, but had the same threshold as those in the control eye. Basal vascular resistances in control:
3" 14 + 0" 32 mmHg min/d-1 (r/ = 28), and diabetic eyes : 3-44 _+0" 19, mmHg min/d 1 (n = 36), were not
significantly different.
Vasoactivity in the early diabetic eye is disturbed with the effective balance between different agonists
altered in favour of catecholamines at physiological concentrations. This may be related to the early
changes in blood flow and oxygen distribution already reported in the rat eye, as well as changes to
autonomic function. The isolated perfused rat eye is a valuable technique for investigating such vascular
reactivity in animal models of retinal disease. © 1995 Academic Press Limited
Key words: diabetes; vascular resistance; isolated perfused eye: rat, catecholamines: 5-HT;
prostaglandins.
1. Introduction
There are numerous reports showing that one
functional consequence of diabetic retinopathy is
alteration to retinal blood flow and also to the
autoregulatory power of the retinal circulation. To
date, despite some speculation, there is no evidence for
accompanying changes to the choroidal circulation.
These retinal circulation disturbances have been
observed in both human diabetics and in animal
models of diabetes (Kohner et al., 1975; Blair and
Riva, 1982, Grunwald et al., 1984, 1986; Small,
Stef/~nsson and Hatchell, 1987; Tilton et al., 1989;
Sullivan et al,, 1990, Bursell et al., 1992; Cringle et
al., 1992). However, there is some controversy
regarding the magnitude and direction of the changes,
possibly due to several factors. These include
differences in the relative time elapsed from diagnosis
or induction of diabetes and the time at which the
* For correspondence.
0014-4835/95/120699 + 13 $12.00/0
experiments are performed and hence the severity of
the disease; the average and peak levels of blood
glucose; the methods used to determine blood flow
such as laser doppler on major retinal vessels
compared to tissue blood flow, or retinal transit time;
and finally species differences.
Recent studies focussed on the initial stages of
diabetic retinopathy have demonstrated early
increases in blood flow values in the retinal circulation
as well as changes to ocular oxygen distribution
within 1-5 weeks after the onset of diabetes in rats as
well as an increase in heterogeneity of retinal tissue
blood flow (Tilton et al., 1989; Alder et al., 1990;
Cringle et al.. 1992). A greater heterogeneity in tissue
blood flow values in the retina, implies a redistribution
of blood flow. Tissue blood flow distribution normally
provides a tight match between blood supply, tissue
demands and the satisfactory removal of the waste
products of metabolism. It is a dynamic, complex and
hierarchical task, The observed redistribution of blood
flow so early in diabetes, well before histological
© 1995 Academic Press Limited