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Anterior Collateral Circulation in the Primate Eye
Anterior Collateral Circulation in the Primate Eye JOHN C. MORRISON, MD, E. MICHAEL VAN BUSKIRK, MD
Abstract: Sequential microdissection and scanning electron microscopy of whole primate ocular lumenal methyl methacrylate corrosion castings were performed to determine the anatomic basis of collateral arterial blood flow to the anterior uvea. Collateral anastomoses were observed at three sites: (1) the episclera where the anterior ciliary arteries interconnect at the limbus to form the episcleral circle; (2) the ciliary muscle where anastomoses between the perforating anterior ciliary and long posterior ciliary arteries comprise the intramuscular circle, the most extensive of the three collateral arterial rings, and (3) the root of the iris where circumferentially oriented vessels derived from the intramuscular circle form the "major arterial circle" . Of these, the "major arterial circle" is the most discontinuous. This multilevel collateral system probably accounts for the rarity of anterior segment ischemia following all but the most extensive extraocular muscle surgeries. [Key words: anterior segment ischemia, episcleral arterial circle, intramuscular arterial circle, lumenal castings, major arterial circle of the iris, scanning electron microscopy.] Ophthalmology 90:707-715, 1983
In 1903, Leber observed that the anterior and long posterior ciliary arteries join at the root of the iris to form the major arterial circle. I Although this circle appears to be the principle site of anterior uveal collateralization, its exact anatomic extent and relationships remain largely unknown because they are obscured from direct observation by the tissue of the surrounding ciliary body. Vascular casting techniques using neoprene and methyl methacrylate provide a unique method for three dimensional analysis of the ocular microvasculature. 2- 9 However, even in these preparations the major arterial circle remains hidden by the dense capillary bed of the ciliary muscle (Fig 1). Scanning electron microscopy of sequentially dissected whole primate ocular microvascular castings has allowed us to determine the precise From the Department of Ophthalmology, The Oregon Health Sciences University, Portland, Oregon, and the Oregon Regional Primate Research Center, Beaverton, Oregon. Supported in part by NIH Research Grant #EY 03279. Presented at the Eighty·seventh Annual Meeting of the American Acad· emy of Ophthalmology, San Francisco, California, October 30-November 5,1982. Reprint requests to E. M.Van Buskirk, MD, Department of Ophthalmology, The Oregon Health Sciences University, 3181 SW. Sam Jackson Park Road, Portland, OR 97201.
interconnections of the anterior and long posterior ciliary arteries and their relationship to the major arterial circle.
MATERIALS AND METHODS Whole ocular microvascular lumenal methacrylate castings were prepared by bilateral carotid artery injection of Batson's compound no. 17 in ten anesthetized old world monkeys (Macaccafascicularis). After allowing the plastic to polymerize, the eyes were enucleated. The tissue was digested away and the resultant castings were prepared for scanning electron microscopy by methods previously described. IO Fifteen castings were hemisected at the equator and the anterior portions mounted on a scanning electron microscope stub, anterior pole facing up. Successively deeper capillary layers were sequentially removed under a 25 to 100X dissecting microscope using a hooked insect dissection needle and Vannass scissors. Critical dissections were performed with a pneumatically powered ultramicroscissors guided by a micromanipulator. At each sequential anatomic level the specimens were studied under an AMR 1000 scanning electron microscope to record the vascular patterns revealed and aid in subsequent dissections. Small arteries
0161-6420/83/0600/0707/$1 .25 © American Academy of Ophthalmology
707
OPHTHALMOLOGY • JUNE 1983 • VOLUME 90 • NUMBER 6
Fig 1. Ciliary body of a primate methyl methacrylate microvascular casting viewed in profile. The major arterial circle (MAC) and other large vessels are mostly hidden within the ciliary muscle capillary bed. CP, Ciliary process; IV, iris vessels (original magnification SOX).
and arterioles were identified by their characteristic fusiform endothelial nuclear impressions. 4 The capillaries and venules of the conjunctiva and Tenon's capsule were first removed to uncover the anterior ciliary arteries and their interconnections within the episclera. These vessels were then severed and removed. The superficia1 layers of ciliary muscle capillaries were next excised to determine the extent of the anterior ciliary arteries as well as the long posterior ciliary arteries after entering the muscle itself. The relation of these vessels to the major arterial circle was examined by removing the deep ciliary muscle capillaries and venules adjacent to the iris root.
episcleral plexus. In this plexus adjacent anterior ciliary arteries interconnect via their lateral-most branches, often forming a complete anastomotic ring within the episclera (Fig 2). Extensions of the remaining anterior ciliary arterial branches perforate the limbal sclera and enter the ciliary muscle (Fig 3). These perforating anterior ciliary arteries number from 10 to 20 per eye and are distributed randomly except for occasional gaps between the rectus muscles. Although the anterior ciliary artery accompanying the lateral rectus participates in the episcleral circle, it directly contributes at most one or two and often no perforating anterior ciliary arteries. In general, the temporal perforating arteries arise from the superior and inferior anterior ciliary arteries.
RESULTS
THE INTRAMUSCULAR CIRCLE
Extensive collateral arterial anastomoses exist at three sites in the anterior uvea: the episclera, the ciliary muscle, and the root of the iris.
Upon entering the ciliary muscle, the majority of the perforating anterior ciliary arteries arborize almost immediately to send multiple arterial branches anteriorly toward the root of the iris (Fig 4). The most lateral of these frequently anastomose with each other and with similar branches from the long posterior ciliary arteries to form the second arterial circle, the intramuscular circle (Fig 5). Although such connections are variable, they
THE EPISCLERAL CIRCLE
After leaving the rectus muscle tendons, the anterior ciliary arteries branch within the episclera to supply the 708
MORRISON AND VAN BUSKIRK •
ANTERIOR COLLATERAL CIRCULATION
Fig 2. Anterior view montage of a left cynomolgus monkey ocular casting with Tenon's and episcleral vessels removed. The anterior ciliary arteries (ACA) arborize at the limbus and interconnect via their lateral branches to form the episcleral circle. CM, ciliary muscle capillary bed; CV, choroidal veins; EC, episcleral circle (original magnification 20X).
are numerous enough to form a complete circle in many eyes. As the remaining perforating anterior ciliary artery divisions approach the iris root they provide capillary branches to the ciliary muscle (Fig 6), and recurrent ciliary arteries that exit the ciliary body and travel posteriorly to supply the anterior choriocapillaris (Figs 5, 7). The latter vessels are randomly distributed and variable in number.
THE "MAJOR ARTERIAL CIRCLE"
Upon reaching the iris root, arterial arborizations from both the perforating antel'ior and long posterior ciliary arteries bend or branch at right angles. Here they travel parallel to the iris root for a short distance before terminating as ciliary process and iris arterioles (Fig 8). These discontinuous circumferentially oriented arteriolar segments comprise the "major arterial circle" which 709
Fig 3. Profile of a perforating anterior ciliary artery as it traverses the limbal sclera to enter the ciliary muscle capillary bed. The fusiform endothelial nuclear impressions (arrow) are characteristic of arteries and arterioles (original magnification SOX).
Fig 4. Posterior view of a cynomolgus ciliary body casting with ciliary muscle capillaries removed. A perforating anterior ciliary artery (arrow) arborizes with most of the branches traveling anteriorly towards the iris root. The "major arterial circle" ("MAC") appears in the background. CV, choroidal veins (original magnification 38X).
MORRISON AND VAN BUSKIRK •
ANTERIOR COLLATERAL CIRCULATION
Fig 5. Anterior view montage of the same eye shown in Figure 2, but with the anterior ciliary arteries and ciliary muscle capillaries removed. Lateral branches of the perforating -anterior ciliary arteries (PACA) and long posterior ciliary arteries (LPCA) interconnect to form a neariy complete anastomosing intramuscular circle (IMC). RCA, recurrent ciliary artery (original magnification 20X).
represents the immediate vascular supply of the iris and ciliary processes. Occasional iris and ciliary process arterioles arise directly from the intramuscular circle as well (Fig 9).
DISCUSSION The anterior uveal circulation in . the primate eye is a highly complex network that interconnects both the anterior and lo'ng posterior ciliary arterial systems. This
results in a potential for collateral blood flow that exists at three levels: the episclera, the ciliary muscle, and the root of the iris (Figs lOA, B). Using neoprene castings, Ashton demonstrated that the anterior ciliary arteries arborized to form an episcleral plexus in addition to the larger perforating branches.3 Our work shows that this plexus joins adjacent arteries and can form a complete anastomosing circle interconnecting all seven anterior ciliary arteries. The second, or intramuscular circle, was first noted 711
Fig 6. Methyl methacrylate casting with partial removal of the ciliary muscle capillary bed. The perforating anterior ciliary artery (PACA) is seen
providing capillaries (arrow) to the ciliary muscle itself (original magnification 95 X).
Fig 7. A recurrent ciliary artery (RCA) ends within the choriocapillaris just anterior to the equator. CV, choroidal vein (Original magnification IOOX).
MORRISON AND VAN BUSKIRK •
ANTERIOR COLLATERAL CIRCULATION
Fig 8. At the iris root, multiple branches from the perforating anterior and long posterior ciliary arteries (arrows) bend or branch at right angles to form the discontinuous "major arterial circle" ("MAC"). Iris veins (IV) can be seen directly entering the choroidal veins. lA, iris artery (original magnification 50X).
by Leber l but has since received little attention as a potential collateral channel. Our findings suggest that of the three anastomotic circles presented here, the intramuscular circle has the greatest anatomic potential to provide anterior uveal collateral flow. In nearly every casting it provided large caliber anastomoses between the long posterior ciliary arteries and adjacent perforating anterior ciliary arteries and in several instances formed a nearly complete anastomosing ring. In addition, it supplies a large portion of the ciliary muscle capillary bed and most of the recurrent ciliary arteries as well as the individual vessels that make up the "major arterial circle." The intimate intraciliary muscular association of the medial and lateral perforating anterior ciliary arteries with the long posterior ciliary arteries explains why simple horizontal rectus surgery has not been associated with anterior segment ischemia in otherwise healthy individuals. II Because the superior and inferior perforating arteries are located further from the long posterior ciliary arteries, they are more dependent on the integrity of the intramuscular circle. The superior and inferior uvea are, therefore, at greater risk following ligation of their respective muscles. This is supported by the observation that isolated tenotomies of the vertical rectus muscles
result in superior and inferior filling delays on iris fluorescein angiography. 12 Characteristically these involve the temporal regions of the iris as well, corresponding to our finding that the vertical anterior ciliary arteries provide most of the temporal perforating anterior ciliary arteries. Talusan and Schwartz have reported limbal fluorescein angiographic evidence that the anterior ciliary arteries fill from inside the eye. 13 Our anatomic data neither confirm nor refute this physiologic finding. It is possible that the large caliber intramuscular circle can permit bidirectional flow in the anterior ciliary arteries depending upon varying physiologic and hydrostatic conditions. Finally, the "major arterial circle" at the root of the iris is the most discontinuous of the three arterial rings described here. Because its individual, circumferentially oriented vessels consistently end as iris and ciliary process arterioles, it is probably less important to collateral flow than previously thought. Instead, collateral blood flow to the anterior uvea depends on all three arterial circles, and it is this redundancy that is responsible for the infrequency of anterior segment ischemia following all but the most extensive extraocular muscle surgeries. 14 ,15 713
Fig 9, An iris artery (IA) arises directly from the intramuscular circle (lMC) (original magnification 95X).
RCA
A
EPISCLERAL CIRCLE
.MC
DISCONTINUOUS 'MAC'
B
Fig 10, A schematic (A) and three dimensional (8) representation of the multilevel collateral circulation in the primate anterior uvea. ACA, anterior ciliary artery; LPCA, long posterior ciliary artery; PACA, perforating anterior ciliary artery; RCA, recurrent ciliary artery; EC, episcleral circle; IMC, intramuscular circle; "MAC", "major arterial circle".
MORRISON AND VAN BUSKIRK • ANTERIOR COLLA TERAL CIRCULATION
ACKNOWLEDGMENT The authors thank Dr. Wolf H. Fahrenbach of the Oregon Regional Primate Research Center for providing laboratory space and access to the scanning electron microscope.
REFERENCES 1. Leber T. Die cirkulations· und Ernl1hrungsverhl1ltnisse des Auges. In: Saernisch T, (Ed.): Graefe·Saemisch Handbuch der Gesamten Au· genheilkunde, 2d ed. Leipzig: Wilhelrn Engelmann, 1903; vol 2, pt 2, Chapter 11. 2. Ashton N. Observations on the choroidal circulation. Br J. Ophthalmol 1952; 36:465-81. 3. Ashton N, Smith R. Anatomical study of Schlemm's canal and aqueous veins by means of neoprene casts. III. Arterial relations of Schlemm's canal. Br J Ophthalmol 1953; 37:577-86. 4. Risco JM, Nopanitaya W. Ocular microcirculation; scanning electron microscopic study. Invest Ophthalmol Vis Sci 1980; 19:5-12. 5. Matsuo N. Scanning electron microscopic studies on the corrosion casts of the blood vessels of the ciliary body. Acta Soc Ophthalmol Jpn 1973; 77:928-35.
6. Ujiie K, Hanyuda T. Three·dimensional angioarchitecture of the pe· ripheral choroid and the ciliary body. Acta Soc Ophthalmol Jpn 1977; 81:662-77. 7. Shimizu K, Ujiie, K. Structure of Ocular Vessels. Tokyo: Igaku-Shoin, 1978. 8. Woodlief NF. Initial observations on the ocular microcirculation in man. I. The anterior segment and extraocular muscles. Arch Ophthal· mol 1980; 98:1268-72. 9. Jocson VL, Grant WM. Interconnections of blood vessels and aqueous vessels in human eyes. Arch OphthalmoI1965; 73:707-20. 10. Van Buskirk EM. The canine eye: the vessels of aqueous drainage. Invest Ophthalmol Vis Sci 1979; 18:223-30. 11 . Jacobs OS, Vastine OW, Urist MJ. Anterior segment ischemia and sector iris atrophy: after strabismus surgery in a patient with chronic lymphocytic leukemia. Ophthalmic Surg 1976; 7(4):42-8. 12. Hayreh SS, Scott WE. Fluorescein iris angiography. II. Disturbances in iris circulation following strabismus operation on the various recti. Arch Ophthalmol 1978; 96:1390-400. 13. Talusan ED, Schwartz B. Fluorescein angiography; demonstration of flow pattern of anterior Ciliary arteries. Arch Ophthalmol 1981; 99;1074-80. 14. Hiatt RL. Production of anterior segment ischemia. J Pediatr Ophthal· mol Strabismus 1978; 15:197-204. 15. von Noorden GK. Anterior segment ischemia following the Jensen procedure. Arch Ophthalmol 1976; 94:845-7.
715
Abstract: Sequential microdissection and scanning electron microscopy of whole primate ocular lumenal methyl methacrylate corrosion castings were performed to determine the anatomic basis of collateral arterial blood flow to the anterior uvea. Collateral anastomoses were observed at three sites: (1) the episclera where the anterior ciliary arteries interconnect at the limbus to form the episcleral circle; (2) the ciliary muscle where anastomoses between the perforating anterior ciliary and long posterior ciliary arteries comprise the intramuscular circle, the most extensive of the three collateral arterial rings, and (3) the root of the iris where circumferentially oriented vessels derived from the intramuscular circle form the "major arterial circle" . Of these, the "major arterial circle" is the most discontinuous. This multilevel collateral system probably accounts for the rarity of anterior segment ischemia following all but the most extensive extraocular muscle surgeries. [Key words: anterior segment ischemia, episcleral arterial circle, intramuscular arterial circle, lumenal castings, major arterial circle of the iris, scanning electron microscopy.] Ophthalmology 90:707-715, 1983
In 1903, Leber observed that the anterior and long posterior ciliary arteries join at the root of the iris to form the major arterial circle. I Although this circle appears to be the principle site of anterior uveal collateralization, its exact anatomic extent and relationships remain largely unknown because they are obscured from direct observation by the tissue of the surrounding ciliary body. Vascular casting techniques using neoprene and methyl methacrylate provide a unique method for three dimensional analysis of the ocular microvasculature. 2- 9 However, even in these preparations the major arterial circle remains hidden by the dense capillary bed of the ciliary muscle (Fig 1). Scanning electron microscopy of sequentially dissected whole primate ocular microvascular castings has allowed us to determine the precise From the Department of Ophthalmology, The Oregon Health Sciences University, Portland, Oregon, and the Oregon Regional Primate Research Center, Beaverton, Oregon. Supported in part by NIH Research Grant #EY 03279. Presented at the Eighty·seventh Annual Meeting of the American Acad· emy of Ophthalmology, San Francisco, California, October 30-November 5,1982. Reprint requests to E. M.Van Buskirk, MD, Department of Ophthalmology, The Oregon Health Sciences University, 3181 SW. Sam Jackson Park Road, Portland, OR 97201.
interconnections of the anterior and long posterior ciliary arteries and their relationship to the major arterial circle.
MATERIALS AND METHODS Whole ocular microvascular lumenal methacrylate castings were prepared by bilateral carotid artery injection of Batson's compound no. 17 in ten anesthetized old world monkeys (Macaccafascicularis). After allowing the plastic to polymerize, the eyes were enucleated. The tissue was digested away and the resultant castings were prepared for scanning electron microscopy by methods previously described. IO Fifteen castings were hemisected at the equator and the anterior portions mounted on a scanning electron microscope stub, anterior pole facing up. Successively deeper capillary layers were sequentially removed under a 25 to 100X dissecting microscope using a hooked insect dissection needle and Vannass scissors. Critical dissections were performed with a pneumatically powered ultramicroscissors guided by a micromanipulator. At each sequential anatomic level the specimens were studied under an AMR 1000 scanning electron microscope to record the vascular patterns revealed and aid in subsequent dissections. Small arteries
0161-6420/83/0600/0707/$1 .25 © American Academy of Ophthalmology
707
OPHTHALMOLOGY • JUNE 1983 • VOLUME 90 • NUMBER 6
Fig 1. Ciliary body of a primate methyl methacrylate microvascular casting viewed in profile. The major arterial circle (MAC) and other large vessels are mostly hidden within the ciliary muscle capillary bed. CP, Ciliary process; IV, iris vessels (original magnification SOX).
and arterioles were identified by their characteristic fusiform endothelial nuclear impressions. 4 The capillaries and venules of the conjunctiva and Tenon's capsule were first removed to uncover the anterior ciliary arteries and their interconnections within the episclera. These vessels were then severed and removed. The superficia1 layers of ciliary muscle capillaries were next excised to determine the extent of the anterior ciliary arteries as well as the long posterior ciliary arteries after entering the muscle itself. The relation of these vessels to the major arterial circle was examined by removing the deep ciliary muscle capillaries and venules adjacent to the iris root.
episcleral plexus. In this plexus adjacent anterior ciliary arteries interconnect via their lateral-most branches, often forming a complete anastomotic ring within the episclera (Fig 2). Extensions of the remaining anterior ciliary arterial branches perforate the limbal sclera and enter the ciliary muscle (Fig 3). These perforating anterior ciliary arteries number from 10 to 20 per eye and are distributed randomly except for occasional gaps between the rectus muscles. Although the anterior ciliary artery accompanying the lateral rectus participates in the episcleral circle, it directly contributes at most one or two and often no perforating anterior ciliary arteries. In general, the temporal perforating arteries arise from the superior and inferior anterior ciliary arteries.
RESULTS
THE INTRAMUSCULAR CIRCLE
Extensive collateral arterial anastomoses exist at three sites in the anterior uvea: the episclera, the ciliary muscle, and the root of the iris.
Upon entering the ciliary muscle, the majority of the perforating anterior ciliary arteries arborize almost immediately to send multiple arterial branches anteriorly toward the root of the iris (Fig 4). The most lateral of these frequently anastomose with each other and with similar branches from the long posterior ciliary arteries to form the second arterial circle, the intramuscular circle (Fig 5). Although such connections are variable, they
THE EPISCLERAL CIRCLE
After leaving the rectus muscle tendons, the anterior ciliary arteries branch within the episclera to supply the 708
MORRISON AND VAN BUSKIRK •
ANTERIOR COLLATERAL CIRCULATION
Fig 2. Anterior view montage of a left cynomolgus monkey ocular casting with Tenon's and episcleral vessels removed. The anterior ciliary arteries (ACA) arborize at the limbus and interconnect via their lateral branches to form the episcleral circle. CM, ciliary muscle capillary bed; CV, choroidal veins; EC, episcleral circle (original magnification 20X).
are numerous enough to form a complete circle in many eyes. As the remaining perforating anterior ciliary artery divisions approach the iris root they provide capillary branches to the ciliary muscle (Fig 6), and recurrent ciliary arteries that exit the ciliary body and travel posteriorly to supply the anterior choriocapillaris (Figs 5, 7). The latter vessels are randomly distributed and variable in number.
THE "MAJOR ARTERIAL CIRCLE"
Upon reaching the iris root, arterial arborizations from both the perforating antel'ior and long posterior ciliary arteries bend or branch at right angles. Here they travel parallel to the iris root for a short distance before terminating as ciliary process and iris arterioles (Fig 8). These discontinuous circumferentially oriented arteriolar segments comprise the "major arterial circle" which 709
Fig 3. Profile of a perforating anterior ciliary artery as it traverses the limbal sclera to enter the ciliary muscle capillary bed. The fusiform endothelial nuclear impressions (arrow) are characteristic of arteries and arterioles (original magnification SOX).
Fig 4. Posterior view of a cynomolgus ciliary body casting with ciliary muscle capillaries removed. A perforating anterior ciliary artery (arrow) arborizes with most of the branches traveling anteriorly towards the iris root. The "major arterial circle" ("MAC") appears in the background. CV, choroidal veins (original magnification 38X).
MORRISON AND VAN BUSKIRK •
ANTERIOR COLLATERAL CIRCULATION
Fig 5. Anterior view montage of the same eye shown in Figure 2, but with the anterior ciliary arteries and ciliary muscle capillaries removed. Lateral branches of the perforating -anterior ciliary arteries (PACA) and long posterior ciliary arteries (LPCA) interconnect to form a neariy complete anastomosing intramuscular circle (IMC). RCA, recurrent ciliary artery (original magnification 20X).
represents the immediate vascular supply of the iris and ciliary processes. Occasional iris and ciliary process arterioles arise directly from the intramuscular circle as well (Fig 9).
DISCUSSION The anterior uveal circulation in . the primate eye is a highly complex network that interconnects both the anterior and lo'ng posterior ciliary arterial systems. This
results in a potential for collateral blood flow that exists at three levels: the episclera, the ciliary muscle, and the root of the iris (Figs lOA, B). Using neoprene castings, Ashton demonstrated that the anterior ciliary arteries arborized to form an episcleral plexus in addition to the larger perforating branches.3 Our work shows that this plexus joins adjacent arteries and can form a complete anastomosing circle interconnecting all seven anterior ciliary arteries. The second, or intramuscular circle, was first noted 711
Fig 6. Methyl methacrylate casting with partial removal of the ciliary muscle capillary bed. The perforating anterior ciliary artery (PACA) is seen
providing capillaries (arrow) to the ciliary muscle itself (original magnification 95 X).
Fig 7. A recurrent ciliary artery (RCA) ends within the choriocapillaris just anterior to the equator. CV, choroidal vein (Original magnification IOOX).
MORRISON AND VAN BUSKIRK •
ANTERIOR COLLATERAL CIRCULATION
Fig 8. At the iris root, multiple branches from the perforating anterior and long posterior ciliary arteries (arrows) bend or branch at right angles to form the discontinuous "major arterial circle" ("MAC"). Iris veins (IV) can be seen directly entering the choroidal veins. lA, iris artery (original magnification 50X).
by Leber l but has since received little attention as a potential collateral channel. Our findings suggest that of the three anastomotic circles presented here, the intramuscular circle has the greatest anatomic potential to provide anterior uveal collateral flow. In nearly every casting it provided large caliber anastomoses between the long posterior ciliary arteries and adjacent perforating anterior ciliary arteries and in several instances formed a nearly complete anastomosing ring. In addition, it supplies a large portion of the ciliary muscle capillary bed and most of the recurrent ciliary arteries as well as the individual vessels that make up the "major arterial circle." The intimate intraciliary muscular association of the medial and lateral perforating anterior ciliary arteries with the long posterior ciliary arteries explains why simple horizontal rectus surgery has not been associated with anterior segment ischemia in otherwise healthy individuals. II Because the superior and inferior perforating arteries are located further from the long posterior ciliary arteries, they are more dependent on the integrity of the intramuscular circle. The superior and inferior uvea are, therefore, at greater risk following ligation of their respective muscles. This is supported by the observation that isolated tenotomies of the vertical rectus muscles
result in superior and inferior filling delays on iris fluorescein angiography. 12 Characteristically these involve the temporal regions of the iris as well, corresponding to our finding that the vertical anterior ciliary arteries provide most of the temporal perforating anterior ciliary arteries. Talusan and Schwartz have reported limbal fluorescein angiographic evidence that the anterior ciliary arteries fill from inside the eye. 13 Our anatomic data neither confirm nor refute this physiologic finding. It is possible that the large caliber intramuscular circle can permit bidirectional flow in the anterior ciliary arteries depending upon varying physiologic and hydrostatic conditions. Finally, the "major arterial circle" at the root of the iris is the most discontinuous of the three arterial rings described here. Because its individual, circumferentially oriented vessels consistently end as iris and ciliary process arterioles, it is probably less important to collateral flow than previously thought. Instead, collateral blood flow to the anterior uvea depends on all three arterial circles, and it is this redundancy that is responsible for the infrequency of anterior segment ischemia following all but the most extensive extraocular muscle surgeries. 14 ,15 713
Fig 9, An iris artery (IA) arises directly from the intramuscular circle (lMC) (original magnification 95X).
RCA
A
EPISCLERAL CIRCLE
.MC
DISCONTINUOUS 'MAC'
B
Fig 10, A schematic (A) and three dimensional (8) representation of the multilevel collateral circulation in the primate anterior uvea. ACA, anterior ciliary artery; LPCA, long posterior ciliary artery; PACA, perforating anterior ciliary artery; RCA, recurrent ciliary artery; EC, episcleral circle; IMC, intramuscular circle; "MAC", "major arterial circle".
MORRISON AND VAN BUSKIRK • ANTERIOR COLLA TERAL CIRCULATION
ACKNOWLEDGMENT The authors thank Dr. Wolf H. Fahrenbach of the Oregon Regional Primate Research Center for providing laboratory space and access to the scanning electron microscope.
REFERENCES 1. Leber T. Die cirkulations· und Ernl1hrungsverhl1ltnisse des Auges. In: Saernisch T, (Ed.): Graefe·Saemisch Handbuch der Gesamten Au· genheilkunde, 2d ed. Leipzig: Wilhelrn Engelmann, 1903; vol 2, pt 2, Chapter 11. 2. Ashton N. Observations on the choroidal circulation. Br J. Ophthalmol 1952; 36:465-81. 3. Ashton N, Smith R. Anatomical study of Schlemm's canal and aqueous veins by means of neoprene casts. III. Arterial relations of Schlemm's canal. Br J Ophthalmol 1953; 37:577-86. 4. Risco JM, Nopanitaya W. Ocular microcirculation; scanning electron microscopic study. Invest Ophthalmol Vis Sci 1980; 19:5-12. 5. Matsuo N. Scanning electron microscopic studies on the corrosion casts of the blood vessels of the ciliary body. Acta Soc Ophthalmol Jpn 1973; 77:928-35.
6. Ujiie K, Hanyuda T. Three·dimensional angioarchitecture of the pe· ripheral choroid and the ciliary body. Acta Soc Ophthalmol Jpn 1977; 81:662-77. 7. Shimizu K, Ujiie, K. Structure of Ocular Vessels. Tokyo: Igaku-Shoin, 1978. 8. Woodlief NF. Initial observations on the ocular microcirculation in man. I. The anterior segment and extraocular muscles. Arch Ophthal· mol 1980; 98:1268-72. 9. Jocson VL, Grant WM. Interconnections of blood vessels and aqueous vessels in human eyes. Arch OphthalmoI1965; 73:707-20. 10. Van Buskirk EM. The canine eye: the vessels of aqueous drainage. Invest Ophthalmol Vis Sci 1979; 18:223-30. 11 . Jacobs OS, Vastine OW, Urist MJ. Anterior segment ischemia and sector iris atrophy: after strabismus surgery in a patient with chronic lymphocytic leukemia. Ophthalmic Surg 1976; 7(4):42-8. 12. Hayreh SS, Scott WE. Fluorescein iris angiography. II. Disturbances in iris circulation following strabismus operation on the various recti. Arch Ophthalmol 1978; 96:1390-400. 13. Talusan ED, Schwartz B. Fluorescein angiography; demonstration of flow pattern of anterior Ciliary arteries. Arch Ophthalmol 1981; 99;1074-80. 14. Hiatt RL. Production of anterior segment ischemia. J Pediatr Ophthal· mol Strabismus 1978; 15:197-204. 15. von Noorden GK. Anterior segment ischemia following the Jensen procedure. Arch Ophthalmol 1976; 94:845-7.
715