Aqueous angiography in pre-glaucomatous and glaucomatous ADAMTS10-mutant canine eyes: A pilot study

Abstract

Objective: To evaluate intravenous scleral and intracameral aqueous angiography in normotensive (n = 4) and hypertensive glaucomatous (n = 6) ADAMTS10-mutant canine eyes.

Animals studied: Ten ADAMTS10-mutant dogs were used in this study.

Procedures: Dogs were sedated and one eye from each dog underwent scleral angiography following intravenous injection of 0.25% indocyanine green (ICG). After a 24-h recovery period, the same eye underwent aqueous angiography via intracameral administration of ICG. Imaging of identical scleral sectors from the same eye was performed using a Heidelberg Spectralis^® Confocal Scanning Laser Ophthalmoscope. Intrascleral vessel depth and lumen diameters were measured using Heidelberg Spectralis^® optical coherence tomography and computer software.

Results: Scleral angiography permitted visualization of vascular components associated with conventional aqueous humor outflow pathways with an average time from injection to fluorescence of 35.8 ± 10.6 s (mean ± SD). Two normotensive eyes (2/10;20%) demonstrated turbulent dye movement, while 4 hypertensive eyes (4/10;40%) exhibited laminar flow. Aqueous angiography demonstrated dye fluorescence within the post-trabecular conventional aqueous humor outflow pathways in all 10 eyes at 34.3 ± 11.0 s post-injection. Sectoral and dynamic outflow patterns were observed primarily within the superotemporal sector in nine eyes (9/10; 90%). Seven eyes (7/10; 70%) demonstrated pulsatile dye movement and five eyes (5/10; 50%) exhibited laminar flow. The degree of laminar movement of dye was greatest in hypertensive eyes. Vessel lumen diameters measured 133.85 ± 28.36 µm and 161.18 ± 6.02 µm in hypertensive and normotensive eyes, respectively.

Conclusions: Aqueous angiography allowed for visualization of fluorescent dye in the superotemporal sclera. Laminar flow and smaller lumen vessels were observed mainly in hypertensive eyes.

Keywords: ADAMTS10; aqueous angiography; canine; conventional outflow; indocyanine green; open-angle glaucoma.

Figure 1.

Standard color image of the temporal sclera of the left eye (A), aqueous angiography of the same area showing the appearance of 0.25% ICG dye fluorescence initially (B) and 20 minutes after IC injection (C), demonstrating progression of dye fluorescence and the presence of laminar flow (arrow) within the scleral vessel over time in a 4-year-old glaucomatous female beagle dog (Dog 3, baseline IOP 27 mmHg).

Figure 2.

Comparison of different imaging techniques (standard color, AA, SA) performed in the temporal sclera in a 1-year-old normotensive ADAMTS10-mutant male beagle dog (Dog 7, baseline IOP 19 mmHg). Standard color image of the temporal sclera in a showing branching of conjunctival vessels (black arrow) (A). Imaging of the same location after IC injection of 0.25% ICG dye yields fluorescence of a deep scleral vessel (B). Scleral angiography, using 1 mg/kg ICG, of the same region confirms the presence of the same deep scleral vessel (arrowhead), along with numerous thinner, branching conjunctival vessels (white arrow; same vessel as depicted in (A) (C).

Figure 3.

OCT imaging was performed in conjunction with aqueous angiography (A, C) and scleral angiography (B, D) in the left eye of a 1-year-old normotensive ADAMTS10-mutant female beagle dog (Dog 6, baseline IOP 19.7 mmHg). Cross-sectional scans (A, B) and longitudinal scans of the scleral tissue (C, D) were performed. The orientation of each scan is indicated by the direction of the green arrows. The presence of scleral vessels in the mid-to-deep stromal tissue were seen in cross section (single arrow, double arrowhead) (A, B) and in longitudinal section (single arrow, single arrowhead) (C, D). Measurements of the vessels were taken through the vertical axis of each vessel lumen, using computer software.

Figure 4.

Bar graph demonstrating vessel lumen diameters (µm) and scleral depth (µm) measured during AA in 12 unaffected wild-type dogs, 4 normotensive and 6 hypertensive ADAMTS10-mutant dogs A reduction in vessel lumen diameter is seen in ADAMTS-10 dogs, which is greater in hypertensive dogs, as compared to wild-type dogs.

Figure 5.

Standard color (SC) images of the temporal sclera of the left eye in 3 different hypertensive ADAMTS10-mutant beagle dogs: a 4-year-old male (Dog 1, baseline IOP 20 mmHg) (A), a 4-year-old male (Dog 2, baseline IOP 31 mmHg) (E), and a 4-year-old female (Dog 3, baseline IOP 27 mmHg) (I) with fluorescence of ICG dye in the deep scleral vessels following aqueous angiography (AA;B, F, J, respectively) and scleral angiography (SA;C, G, K, respectively). Scleral angiography demonstrates the presence of a complex branching pattern of deep scleral vessels, with thinner, superficial conjunctival vessels in the overlying tissue. Color maps were made to show simultaneous SA and AA results for each ADAMTS10-mutant dog (D, H, L); AA highlights ICG fluorescent patterns in red, while SA is depicted in blue.