Quantitative Morphology of Human Retrolaminar Optic Nerve Vasculature

Jane M. Olver,*^ D. J. Spalton,X and A. C. E. McCartney^

Purpose. To quantify the variation in the blood supply of the retrolaminar optic nerve in humans. The retrolaminar anterior optic nerve is supplied by an elliptical arterial "circle" of Haller and Zinn formed by anastomoses around the optic nerve between medial and lateral paraoptic short posterior ciliary arteries (PO-SPCAs). The frequency with which complete perioptic nerve arteriolar anastomoses (PONAA) occur is unknown, yet they form the basis for many postulated pathophysiological mechanisms. Methods. Scanning electron microscopy was performed on 25 orbital and ocular microvascular corrosion casts (methyl methacrylate) from 20 human cadavers of subjects 21 to 97 years of age without known ocular disease. Results. Eighteen casts were examined in detail after microdissection (the analysis of seven casts was limited because of their fragility). In 15/18 (83%) casts, the PONAA were supplied by branches of a medial and lateral PO-SPCA; in 2/18, they were supplied by one (lateral) PO-SPCA; and in 1/18, they were supplied by a superior PO-SPCA and two horizontal PO- SPCAs. The PONAA had intact superior and inferior anastomoses in 8/18 (44%) casts, complete anastomoses with narrowed portions in 6/18 (33%), and incomplete in 4/18 (23%). Narrowed portions were not preferentially distributed to either superior or inferior anastomoses. Conclusions. Complete PONAA was found in more than 75% of casts, including anastomoses with narrow portions in 33% of casts. Invest Ophthalmol Vis Sci. 1994; 35:3858-3866.

J. he vascular structure of the retrolaminar optic centripetal arterioles, and centripetal branches of re- nerve in humans after histologic serial sectioning, current choroidal arterioles derived from the methyl methacrylate casts, and other injection tech- PONAA.6 Such anastomoses are absent in subhuman niques has been described.1"7 We have shown that primates.9"11 Variations in the blood supply of the an- anastomoses between medial and lateral paraoptic terior optic nerve have been noted in humans.12 In short posterior ciliary arteries (PO-SPCAs)6'7 form an this study, we examined the variation in origin and elliptical "circle" consisting of superior and inferior form of the PONAA using methyl methacrylate tech- parts around the optic nerve. The perioptic nerve arte- niques. Quantitative analysis may help establish riolar anastomoses (PONAA) are similar to the circle whether variations in vascular structure determine pat- originally described by Haller and Zinn in 1755.8 In terns of visual field loss in conditions such as anterior humans, the retrolaminar and laminar optic nerves ischemic optic neuropathy. receive their blood supply from pial arterioles, direct

METHODS From the * Moorfields Eye Hospital, the f Department of Pathology, Institute of Ophthalmology, and the \Department of Ophthalmology, St. Thomas' Hospital and Microvascular Casting Techniques in Humans Guy's Hospital, I^ondon, United Kingdom. Presented at the annual meeting of the Association for Research in Vision and Complete orbital and ocular microvascular corrosion Ophthalmology, Sarasota, Florida, April 1991. Supported by the Francis and Renee Hock Trust and by the Special Trustees of casts were prepared from 25 adult human autopsy Moorfields Eye Hospital (/MO). specimens (20 cadavers) obtained 36 to 48 hours after Submitted for publication fanuary 12, 1994; revised March 16, 1994; accepted 13 May 12, 1994. death using our standard techniques. The autopsy Proprietary interest category: N. specimens were collected from St. Thomas' Hospital. Reprint requests: Dr. Jane M. Olver, Moorfields Eye Hospital, City Road, London EC1V 2PD, England. Hospital ethical committee approval was granted for

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TABLE l. Short Posterior Ciliary Artery TABLE 2. Composition of the PONAA Supply of the PONAA ("Circle" of Haller ("Circle" of Haller and Zinn) and Zinn) Number of Percentage of Number of Percentage of Casts Casts Casts Casts Complete anastomoses 44 Medial and lateral para- Complete with optic SPCAs 15 83 narrowed sections 33 Lateral para-optic SPCA 2 11 Incomplete anastomoses Medial, lateral, and (including 1 fractured superior SPCAs 1 6 anastomosis) 23 n = 18 casts. the lid-sparing exenterations. Casting was achieved by injection of low viscosity methyl methacrylate resin taya's method14 was used, and in four eyes Fahren- mixture through the ophthalmic artery at its origin bach's method was used.15 All the surrounding tissue from the carotid artery (perfusion pressures of 125 to was corroded in 6 M potassium hydroxide, and the 175 mm Hg). In 21 eyes, a modification of Nopani- casts were thoroughly washed in distilled water and then air dried. Examination of Vascular Casts Each cast was examined under a binocular dissecting microscope to orientate the specimen and to identify the posterior ciliary bundles and perioptic nerve arteriolar anastomoses (PONAA). Microdissection was performed to reveal details of the blood supply to the retrolaminar and laminar optic nerve regions. The dissected specimens were mounted on aluminum stubs and were coated with gold sputter (50 ^m gold) for examination under scanning electron microscopy at 20 kV. Photographic documentation of nine different views of each microvascular cast was made at mag- nifications X20 and X25 by rotating and tilting the specimen within the scanner. Detailed documentation of features of interest was made at higher magnification.

RESULTS Full analysis of 7/25 casts was limited by fragility on sequential microdissection; therefore, the findings for these casts are not included. There were 14 white subjects—five men and nine women, 21 to 97 years of age (mean, 71 years; median, FIGURE l. Scanning electron photomicrograph montage. 76.5 years). In 10 of these subjects, only one eye was Posterior view of a methyl methacrylate cast of a left human studied. All eyes were from subjects without known globe, showing easily recognizable vortex veins and outer ocular disease, as determined by telephone discus- choroidal vessels. Medial (on right of optic nerve) and lat- sions with relatives and by hospital records if available, eral (on left of optic nerve) short posterior ciliary artery with full ethical committee approval from St. Thomas' bundles are composed of distal and paraoptic short poste- Hospital. Refractive errors were not recorded. Mor- rior ciliary arteries. A medial and a lateral paraoptic SPCA phometric findings are summarized in Tables 1 each divides into superior and inferior branches diat form and 2. a microscopic anastomosis above and below the optic 3lf> 7 nerve. ' The term perioptic nerve arteriolar anastomoses Overview of Short Posterior Ciliary Circulation (PONAA) is used instead of circle of Haller and Zinn in the text. Here, the PONAA is complete but has narrowed A montage depicting the medial and lateral short pos- sections. terior ciliary artery bundles is shown in Figure 1. Each

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FIGURE 2. (A) Scanning electron micrograph of a methyl methacrylate cast of a right human eye (same eye as in Fig, 3, eye 1R, but viewed obliquely from a 90° angle). This is an oblique view of part of the medial SPCA bundle (on left), with the inferior branch of the medial paraoptic SPCA branch contributing to the inferior anastomosis (boxed). Bar = 600 ^m, (B) Higher magnification of boxed part of (A) showing pial arteriole (asterisk [*]) and its branches encircling and entering the anterior optic nerve {arrow) supplying the retrolaminar optic nerve. Solid circles indicate a pial vein. Bar = 100 pm.

bundle is composed of many distal short posterior different angles) are shown in Figure 3. Scanning elec- ciliary arteries (D-SPCAs) and one paraoptic short pos- tron micrographs of one cast seen from two different terior ciliary artery (PO-SPCA) lying closest to the op- angles, including magnified details of branches, are tic nerve.3 The lateral PO-SPCA most commonly di- shown in Figure 4. vides proximal to the medial PO-SPCA (estimated ex- In 15/18 (83%) of casts, the PONAA was supplied trascleral), adjacent to the anterior optic nerve, with by both a medial and a lateral PO-SPCA, whereas in a characteristic gap between it and the more numer- 2/18 (11%) casts it was supplied by a lateral PO-SPCA ous D-SPCAs in the lateral bundle (Fig. 1). The medial (Fig. 5) and in one eye it was supplied by a superior PO-SPCA branches more distally (estimated to be ei- SPCA and two horizontal PO-SPCAs (see Table 1). ther just outside the sclera or within the sclera), close The PONAA was complete in 14/18 (77%) of casts to the D-SPCAs, without a discernible gap (Fig. 1). with both superior and inferior anastomotic parts. The location of branching in relation to the sclera However, in six (33%) of these casts, narrowed sec- is estimated by the distance posterior to the choroid tions (Figs. 1 and 6) were noted that were not re- because all tissue landmarks are corroded in vascular stricted preferentially to either the superior or the casting. The medial and lateral PO-SPCA branches inferior parts (see Table 2). For example, in the left form a "circle" of Haller and Zinn composed, in ef- eye of subject 3 (Fig. 1), there were narrow sections fect, of two anastomotic parts, one superior and one along both the superior and the inferior anastomotic inferior to the anterior optic nerve, which are better parts, and in the right eye of subject 8 (Fig. 6), there termed perioptic nerve arteriolar anastomoses was a narrow section in only the inferior part of the (PONAA). The retrolaminar optic nerve is supplied by pial arterioles arising from the PONAA (Fig. 2). anastomosis. A narrow portion was denned as a small, Other branches from the PONAA include recurrent interconnecting vessel of regular but narrow caliber choroidal arterioles and centripetal arterioles. (20 to 30 {im intraluminal diameter) completing the PONAA. Pial arterioles and direct centripetal Specific Vascular Findings branches still arose from narrow portions. Narrowings Scanning electron micrographs from one view of five were not noted elsewhere in the casts. of the 18 casts (each cast was examined from nine In 4/18 (22%) casts, the PONAA was incom-

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FIGURE 3. Five scanning electron micrograph "minia- tures" at various stages of microdissecdon, each viewed posteriorly. Padent number and laterality are marked on the micrograph. Original magnificadon, X20. Eyes 2R and 3R show PONAA detached from the choroid and the optic nerve. Eye 3R is viewed anteriorly. An iatrogenic break is seen along the anastomosis in the upper figure. Bar = 1200 \i. All casts were examined from eight additional views to establish die supply and form of the PONAA, which cannot always be seen from this one view.

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FIGURE 4. (A) Inferior view of left eye of subject 7 (same cast as Fig. 3, no. 7L) showing complete inferior anastomosis {large solid white arrow) between vertically orientated lateral paraoptic SPCA {small white arrows) and flatter orientated medial paraoptic SPCA branches {black arrows). Bar = 600 fxm. (B) Posterior view of the same eye showing branches of medial paraoptic SPCA (black arrows). On the left lies part of the optic nerve with both the central retinal vein (V) and the artery (A). Bar = 325 //m. (C) Lateral view of same eye showing lateral paraoptic SPCA in foreground (star) dividing into three branches, one superior (white solid arroxu) and two inferior branches (solid black core arrow). Central retinal artery (A), central retinal vein (V) in center of optic nerve capillaries. Bar — 325 fim. (D) Higher magnification of part of inferior anastomosis (lying horizontally in lower picture) with pial arterioles (asterisks [*]), direct centripetal branches (small open arrows), and centripetal branches (small solid black arrows) off recurrent choroidal arterioles supplying the retrolaminar and laminar optic nerve. Bar = 100 (j,m.

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proportion (12%) either one or three paraoptic short posterior ciliary arteries contributed. Although the anterior optic nerve in humans is largely supplied by the short posterior ciliary circulation, apart from the surface nerve fiber layer, most of the short posterior ciliary circulation supplies the choroid; the anterior optic nerve is usually supplied by two paraoptic SPCAs, which also supply the peripapillary choroid, whereas the 10 to 20 distal SPCAs supply only the choroid. On the rare occasions when only one PO-SPCA supplies the anterior optic nerve, there may be potential vascular vulnerability, similar to a "circle" of Willis (circulus arteriosus of Willis) with only one internal carotid artery. The casting techniques used in this study involve complete tissue corrosion and extensive manipulation and therefore are limited by fragility, making accurate quantitative analysis of smaller vessels, particularly capillary densities, difficult. Although the low viscosity of the mixture appears to give a good capillary and ve- nous fill, such vessels may be lost again during pro- cessing and dissection. For instance, in this series, one of the four casts (22%) in which the "circle" was FIGURE 5, Complete PONAA dissected from the posterior incomplete had an apparent iatrogenic fracture, with choroid and anterior optic nerve (same cast as Fig. 3, eye loss of a small section of the circle of Haller and Zinn. 2L). It is supplied by only one lateral paraoptic SPCA {open These fractures are usually apparent from the shape arrow). Although this appears to be similar to a circle, it of the broken ends on scanning electron microscopy. could not function as one. Bar = 750 /im, Care must be taken in interpreting empty areas in casts, particularly when specimens with suspected disease are being examined. Comment can only be made plete—that is, the superior or inferior (or both) anas- on microvascular casts that are present. The cast with tomosis was not continuous. However, in one cast (Fig. an obvious fracture and a missing segment may have 3, right eye of subject 3), there was an obvious break had complete anastomosis. in the inferior part because of damage, and it was Other methyl methacrylate casting studies4"6 have impossible to say whether the PONAA in this cast had confirmed the presence of some form of arterial circle originally been complete. In two casts, the anastomosis around the anterior optic nerve in humans. Investiga- was incomplete in either its superior or its inferior tions of latex casts of human eyes were not primarily part. In the cast with a tripartite SPCA blood supply, designed to examine the anterior optic nerve, which it was incomplete in two locations. was often discarded to allow for choroidal and anterior uveal studies.16"18 Interpretation of latex casts was hampered by the low magnification and depth of fo- DISCUSSION cus of dissecting microscopes and by the difficulty in This methyl methacrylate vascular casting study of hu- distinguishing accurately between arteries and veins man eyes (without known ocular disease) clearly dem- and the lack of rigidity of the cast. These problems onstrates the variation in the blood supply to the retro- have been redressed in methyl methacrylate casting, laminar and laminar regions of the anterior optic wherein high magnification and depth of focusing are nerve. Although the "circle" of Haller and Zinn in available with scanning electron microscopy and the man was originally described in 1755 from meticulous type of vessel is identifiable by the characteristic endo- dissections of human cadaver eyes, the frequency of thelial nuclear impressions made on the rigid its existence and its form has remained unclear. In this cast. 13,14,19,20 study, perioptic nerve arteriolar anastomoses between Findings from studies using histologic serial sec- 1 PO-SPCAs were present with intact superior and infe- tions are difficult to interpret because the rior parts in 77% of the casts examined, although in PONAA lies in different planes anteroposteriorly (like several of these the anastomoses had narrow portions. a hammock) and has both extrascleral and intrascleral Branches of two PO-SPCAs (medial and lateral) most portions. The three branches derived from the commonly formed the anastomoses, but in a small PONAA are pial, recurrent choroidal, and direct cen-

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tripetal. It is not possible to distinguish between arter- The term circle of Haller and Zinn may imply ies, arterioles, and terminal arterioles other than by both an anatomic and a functional vascular circle. The the cast diameter, which represents the vessel lumen "circle" is an ellipse consisting of two separate ana- diameter because all tissue has been corroded. The tomic anastomoses between branches of a medial and histologic distinction between a small artery and a a lateral PO-SPCA, and the patterns of vascular large arteriole is arbitrary, and we have named the pial branching and reduction of intralumenal diameter branches arterioles and recurrent choroidal branches along the anastomoses do not suggest that these vascu- arterioles by their cast diameters. Three-dimensional lar anastomoses function as a circle. A similar semantic reconstruction of these from histologic serial sections argument can be applied to the term circle of Willis is difficult because the blood vessels branch in differ- (circulus arteriosus of Willis), which also does not ent directions from the anastomotic parts of the circle function as a circle. We are, therefore, increasingly (Fig. 4d). The pial arterioles pass first centripetally, using the term perioptic nerve arteriolar anastomoses. then proximally, along the pia, supplying the retro- Under normal physiological conditions, it appears un- laminar optic nerve (Figs. 2, 4, and 6). The recurrent likely that blood would flow into one PO-SPCA, cross choroidal arterioles are so named because they pass the anastomosis, and exit through the other PO-SPCA. centripetally and anteriorly before bending sharply to It is likely that an arterial front exists along each anas- travel in a centrifugal anterior direction to supply the tomosis, where blood from each of the two PO-SPCAs peripapillary choroid. Pial and direct centripetal arte- meets, then runs off in the branches to the retrolami- rioles from both the PONAA and the elbow of the nar and laminar optic nerves, and to the peripapillary recurrent choroidal arterioles supply the retrolaminar choroid. This zone of functional separation of flow and laminar optic nerves. Neither the numbers of pial from the medial and lateral PO-SPCA may be regarded arterioles derived from each part of the PONAA nor as a functional watershed zone, which may shift along the capillary densities of retrolaminar and laminar op- each of the anastomoses according to the relative per- tic nerves were quantified for this study. fusion pressures, varying, for instance, with eye move- Levitzky and Henkind,22 from studies combining ments even though there is anatomic continuity along histologic sectioning and ink injection techniques, the vascular anastomoses. It is interesting that in one suggested that the circle of Haller and Zinn was in- third of the casts studied, narrow segments were found complete in most instances. Lieberman et al1 com- along one or both vascular anastomoses that were mented that intrascleral anastomoses were variable in shown to be continuous with vessels from the other extent and number and did not report a complete PO-SPCA when the specimen was tilted and rotated circle in humans. Using dissection and latex casts, in the scanning electron microscope. It should be Hayreh12'23 examined large numbers of human ca- noted that these attenuated sections were located to daver orbits and concluded that the circle of Haller one side of the midline, the significance of which is and Zinn was most commonly incomplete. Some stud- unclear. These narrow portions probably do not repre- ies failed to differentiate clearly between findings from sent vessel spasm in view of the timing of casting after humans and other primates.21'22 Anderson and Braver- death. Neither do they represent postmortem clot by man10 clarified this by showing that some form of anas- their morphologic appearance. An artefact cannot be tomotic intrascleral circle was found in human speci- excluded. The PONAA were often anatomically com- mens, but not in subhuman primates. Risco et al,11 plete, but this does not mean they were functionally working with methyl methacrylate casts of cynomolgus complete. monkeys, confirmed that SPCA branches supplied the Although the pathogenesis of anterior ischemic distal optic nerve, without any anastomoses between optic neuropathy is unknown, an understanding of SPCAs. A review of the literature and the results of the blood supply of the retrolaminar optic nerve may this study show that although morphologic findings in help in understanding the different clinical and fluo- humans are similar to those found in other primates, rescein angiographic appearances of arteritic and caution should remain in extrapolating findings from nonarteritic anterior ischemic optic neuropathy.24"26 subhuman primates to man. Such comparisons may In nonarteritic anterior ischemic optic neuropathy, also be limited because subhuman primate studies hypoperfusion within the microvasculature of the an- have usually been undertaken on live or freshly killed terior optic nerve affects the microperfusion of the young healthy animals, whereas most human ana- retrolaminar optic nerve.6 Ischemia may occur in an tomic studies are autopsy specimens from older sub- anatomically crowded disc with a tight scleral canal jects with a range of ages (and hence arteriosclerosis) and a thickened sclera.27 There may be associated peri- examined many hours after death. Increasing age did papillary choroidal perfusion delay on fluorescein an- not appear, in this study, to be related to incom- giography.26 In contrast, occlusion of the posterior pleteness of the circle because some of the complete and short posterior ciliary arteries from arteritis28 not anastomoses were found in older subjects. only causes an infarct in the optic disc, it also produces

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