Eye (1988) 2, 533-546

Patterns of Blood Flow in Episcleral Vessels Studied by Low-Dose Fluorescein Videoangiography.

PAUL A. R. MEYER

Camhridge

Summary The blood supply of the ocular anterior segment arises from a saggittal arterial ring composed of the long posterior ciliary , the muscular and anterior and perforating scleral arteries. This ring supplies coronal arterial circles within and outside the globe. Low dose anterior segment fluorescein videoangiography demonstrates arterial and venous flow, recording its characteristics and direction. Videoangiograms were performed at low and high magnification in 15 normal subjects. Episcleral arteries and were distinguishable by the presence or absence of pulsatile flow and by their fluorescence intensity. Arteries usually perfused earlier than veins, and with higher flow velocity. Twenty-five of 40 arteries flowed away from scleral perforations close to the limbus. All 8 veins drained away from the limbus. The communication between two arteries may be demonstrated by a static, pulsating column of non-fluoresceinated blood. This sign arose at a point of scleral perforartion, at the junction between muscular and anterior ciliary arteries and in the episcleral arterior circle. It supports the concept of arterial shunting, both in the saggittal plane and in the superficial coronal circle. Perforating scleral arteries lay anterior to the episcleral arterial circle in superior angiog­ rams and posterior to it in inferior studies. Vessels that had been characterised by video angiography were identified in stereo colour photographs of angiographic fields. Arteries were best distinguished from veins by their high tortuosity and thick walls. Using these photographic characteristics, the distribution of arteries and veins over the rectus muscles was surveyed in 13 subjects. The incidence of arteries is lowest over the . Veins were concentrated in the vertical meridian and were absent over lateral rectus in 8 SUbjects. Five intra-operative videoangiograms are reported. Retraction of facilitated imaging of the episcleral vessels and demonstrated arterial communication through a shared bed.

Although the vessels of the ocular anterior this circulation. His findings have since been segment comprise the most accessible circu­ embellished by indian ink injections 2 and lation in the body, controversy surrounds the dissections of vascular castings. 3.4.5,6 patterns of blood flow within them. On the surface of the eye the muscular The brilliant dissections of Leberl form the arteries, which arise from the ophthalmic foundation for our current understanding of ?, run forward as the anterior ciliary

Correspondence to Paul A.R. Meyer, Department of Ophthalmology, Addenbrooke's Hospital, Cambridge.

Presented at the Annual Congress of the Ophthalmological Society of the United Kingdom, April 1988. 534 P. A. R. MEYER arteries 1 and meet in an anterior episcleral cate by perforating branches of the anterior arterial circle (eac. ). 6.8 This feeds the ciliary arteries.5,6 The potential therefore anterior conjunctival and episcleral capillary exists for an elaborate arterial shunt system, beds8. Within the globe the medial and lat­ in which two coronal arterial circles, one eral long posterior ciliary arteries, which also within and one outside the globe, are arise from the ophthalmic artery 7, supply the supplied and joined by a saggittal arterial "major circle of the iris" . 1,5.6 This is thought ring (Fig. 1). to distribute blood to the ciliary body, iris In order to clarify the routing of blood and anterior choroid5. through this system, many authors have The intra-ocular arterial circles may be examined the direction of flow in photo­ more variable and fragmented than Leber graphic fluorescein angiograms of anterior believed9, and methacrylate castings of pri­ ciliary vessels. Bron and EastyJO, Amalric, mate anterior segment vessels6 indicate that Rebiere and Jourdesll, Ikegami, Talusan and it has two components: one at the root of the Schwartzl3 and Watson and Boveyl4have all iris and one within the ciliary muscle itself. collected angiograms of large episcleral ves­ The two anterior arterial circles communi- sels that penetrated the sclera close to the limbus, and in which blood flow appeared to be centrifugal. However, the interpretation of their results is complicated by the presence of "emissary veins" that cross the supra-choroi­ dal space and perforate the sclera, draining the iris and ciliary body circulations into the episcleral venous system. 2 Ikegami, and Talusan and Schwartz asserted that perforat­ ing centrifugal scleral vessels were anterior ciliary arteries, but Almaric et al. and Bron and Easty considered them to be "emissary veins". Photographic anterior segment has been subject to two impor­ tant constraints: fluorescein extravasation may interfere with documentation of the capillary and venous phases, and the slow recycling rate of flash units restricts observa­ tions on flow characteristics or direction. Both these problems are overcome by low dose anterior segment fluorescein videoan­ giogaphy. Fig. 1. Arterial communications in the anterior seg­ Intravascular fluorescein binds ionically to ment of the globe. circulating albumin 15.16 and, by restricting the oa - ophthalmic artery dose to avoid saturating this system, fluores­ ma - artery of rectus muscle cein leakage may be considerably reduced. 8 aca - anterior ciliary arteries (joined by episcleral Since a video camera captures 25 frames arterial circle) per second, each of which is composed of two lpca - long posterior ciliary artery fields, the direction of flow with velocity of ec - episcleral up to 400mm/sec. can theoretically be deter­ mc - muscular capillaries C> - intraocular arterial circle (major circle of iris) mined in an 8mm diameter field (assuming

• - extraocular arterial circle (anterior episcleral arte­ uniform illumination, a sharp fluorescein rial circle) front and no camera sensitivity threshold). note: ma + aca + scleral perforator +lpca form Flow characteristics such as pulsatility are saggittal arterial ring. also demonstrated. PATTERNS OF BLOOD FLOW IN EPISCLERAL VESSELS 535

Videoangiography does pose technical the second angiogram at "x16" magnification problems. Continual illumination of the eye (8mm/vertical screen). The subject looked demands a lower intensity of exciting radia­ ahead during the first angiogram: subsequent tion, there is consequently less fluorescence, angiograms at "x16" were performed at and a very sensitive video camera is required. extremes of horizontal or vertical gaze. As a result, intensified silicon target (ISIT) In three subjects 3 additional angiograms cameras have been used for posterior seg­ were performed at "x16" magnification, to ment fluorescein video angiography. 17.18 complete a survey of the anterior globe. During anterior segment fluorescein The anterior segment vasculature of each angiograms, low fluorescence is compounded eye was also recorded on colour reversal film by the need to restrict the dose of (Echtochrome, ASA 200): a survey of the fluorophore. A further complication is the whole anterior segment circulation was made very high fluorescence that accrues late in the at "xlO" and stereo pairs were taken of every angiogram as a result of fluorescein leakage angiographic field. from conjunctival and episcleral capillaries. This requires the camera to tolerate a range Videoangiography Recording Technique of luminance far greater than an ISIT camera Angiograms were performed on a Ziess clini­ can accomodate. cal slit lamp. Excitation of flourescence was These requirements are satisfied by "sec­ by a 25 watt tungsten source with a 450- ond generation" image intensifiers. The 490nm band-pass interference filter, and a image is formed on a photocathode, from long pass barrier filter (T50:515 nm) was which electrons are accelerated and focussed placed in the imaging light path. onto a micro-channel-plate. This acts as a For video recording the image was two-dimensional array of photomultipliers, reflected by a 50/50 beam splitter onto the which further accelerate the electons to photo-cathode of a second generation image excite an output phosphor. The recreated intensifier (Mullards XX1500), fibre-opti­ image can be recorded by a sensitive monoc­ cally coupled to a Nuvicon monochrome hrome video camera. camera (Visual Contacts). The photocathode The present study uses this technology to potential of the image intensifier was control­ establish patterns of arterial perfusion and led manually and the camera was modified to venous drainage in the anterior segment of give linear electronic gain. the . This is essential for a clear Images were stored on low-band U-matic understanding of ocular physiology and for videotape. For analysis they were transfered the rational design of surgical procedures. with a time-base onto 1 inch videotape, slowed to one fifth real time and re-recorded SUBJECTS AND METHODS in U-matic format. Episcleral Fluorescein Videoagiography The still reproductions in this paper were Without Intervention prepared by grabbing paused frames from Subjects the original tapes into a digital frame store Fifteen normal subjects participated: eight (Supernova). females and seven males. Their ages ranged from 23 to 62 years. All gave informed con­ Procedure sent. Each angiogram was preceded by a 30sec. ' The right eye was studied in six subjects video sequence of the selected area, allowing and the left eye in nine. Each participant an appropriate image intensifier gain setting underwent two angiograms, separated by an . to be selected. This was chosen to be the low­ interval of more than twenty-four hours: the est gain that gave a negative image of vessels first included the inferior, nasal and temporal against background scleral auto- or pseudo - episclera at "xlO" magnification (13mm/ver­ fluorescence. The camera settings (electronic tical screen). From this field an area of gain and black level) were not changed bet­ interest including the limbus, and at least one ween subjects. major anterior ciliary vessel, was selected for The position of any pseudofluorescence 536 P. A. R.MEYER was determined from the control sequences, lacked any run-off. Observations upon and artefacts arising from light reflexes were arteries were confined to systole. recorded by displacing the light source. The position of the fluorescein column was Sodium fluorescein (1. 5mg per kilogram recorded on a paused frame and the number body weight) was then injected rapidly into of fields that elapsed before the column an anti-cubital fossa vain. The recording con­ reached a second, predetermined position tinued throughout the circulation time and were recorded. The sequence was then con­ the arterial, capillary and venous phases of tinued until the vessel had perfused fully the angiogram. It was terminated when before the length between the two points fluorescein lejlkage had negated all positive were measured with dividers. Corrections vascular images. were made for magnification on the monitor.

Interpretation of Angiograms The low power videoagiograms were At present videoangiography does not examined to determine gross patterns of achieve the same resolution as photographic episcleral and conjunctival perfusion, and to imaging and the interpretation of capillary select areas suitable for further investigation. detail was often restricted. Where possible (5 The directions of flow within large vessels angiograms), the origin and drainage of were noted wherever possible and compared capillaries were recorded, but no attempt was with those undertaken at extremes of gaze. made to estimate systolic flow velocity. In the All quantitative work was performed upon remaining angiograms, study of the microcir­ angiograms that had been recorded at high culation was limited to the recording of fields magnification. of perfusion.

Intra-Operative Videoangiography of Large Vessels Episclera All vessels that were well focussed, and Angiograms of exposed muscular and imaged with adequate contrast, were drawn episcleral vessels were performed in five on a flow diagram, and where possible their adult subjects during cataract or det�chmenr depth was found from stereo colour photo­ surgery. The superior rectus was examined in graphs. three patients and studies were also per­ formed over the inferior and lateral recti. Perfusion Characteristics Conjunctiva over the region to be The angiographic sequence was timed from examined was retracted using the minimum the first appearance of intravascular fluores­ possible dissection and cautery. Muscles cein. were relaxed, and no attempt was made to The following criteria were recorded for at measure or correct intra-ocular pressure. least six vessels in each angiographic field: The angiography proceedure was similar to (1) The moment of first perfusion with that described above. Off-axis illumination of fluorescein. the operating field was provided by a 50 watt (2) The presence or absence of pulsatile (dis­ quartz-halogen light source, transmitted by a continuous) flow. fibre optic light guide fitted with a condenser. (3) Fluorescence intensity (analogue scale 0- A 50/50 beam splitter, mounted on a Zeiss 3, where O=no positive image; 3=satura­ operating microscope, directed the image tion of grey scale). through the long-pass barrier filter onto the (4) Flow velocity and direction (whenever photocathode of the image-intensified video possible). camera. The fluoresceindose was 2. 0 mg/kg.

Flow Velocity Identification of Vessels in Colour Flow velocity was estimated only in stretches Photographs of vessel that demonstrated a sharp fluores­ Where possible, the large radial vessels in cein front, were more than 4mm long and which videoangiographic flow characteristics PATTERNS OF BLOOD FLOW IN EPISCLERAL VESSELS 537

had been recorded were identified in the tolic flow velocity was very variable (1. 6 - stereo colour photographs of angiographic 100mmlsec�), but all high velocity vessels fields. Their photographic appearances were were in this group. scored as follows: (II) Major vessels that filled after the arterial (1) tortuosity (the least angle between tan­ flow phase in the field concerned were usu­

gents to the circumference of a bend was ally less fluorescent ( = 2 on analogue scale), measured (Fig. 3); radius of curvature was and sometimes distinguishable only by the

not considered. <900 = high; >900 = low). loss of their vascular silhouette. Their flow (2) Wall thickness (1-3, where visible blood was not pulsatile.

column = 1; vessel elevated when viewed Vessels with these characteristics were

stereoscopically = 3). considered to be veins. They filled gradually (3) Streaming of blood (+/-). and with a diffuse fluorescein front, hence Having established photographic charac­ the moment of their first perfusion, their flow teristics arteries and veins, the vessels seen in direction and velocity were difficult to ascer­ 3600 photographic surveys of 13 normal eyes tain. When this was possible, flow velocity were identified and drawn. The incidence of «4. 3mmlsec.) was usually lower than within episcleral arteries and veins at each rectus adjacent arteries. muscle insertion was recorded. Photographic Appearance (Fig. 3) Results It was possible to record all the chosen Gross Perfusion Patterns angiographic and photographic criteria in 50 The whole globe did not fluoresce simultane­ large radial vessels from 18 high power ously: The episclera was perfused in a angiograms. These had been performed in 14 number of discrete fields which filled at inter­ subjects, two of whom contributed 3 studies. vals of up to 13.5 seconds. Although pigment Thirty five vessels with the angiographic may interfere with the iris angiogram, perfu­ characteristics of arteries were found to have sion of the iris was seen to precede that of the thick walls and high tortuousity. One, though episclera in 4 of the 15 studies. thick-walled, was not tortuous. The anterior perfusion fields were usually Seven vessels with the angiographic centred upon single or grouped perforating characteristics of veins had low tortuosity and episcleral arteries that flowed away from the thin walls. One , which emerged from limbus and towards the rectus muscles. When the sclera and received other episcleral veins, . grouped, vessels at the centre of a field had low tortuousity but thick walls. fluoresced simultaneously. Adjacent fields Six vessels (from 2 subjects) had high tor­ were joined by the episcleral arterial circle tuousity and thick walls, but filled late in the (eac. ), which supplied the intervening episcl­ angiogram. In one subject, both vessels with era (Fig.5). these characteristics demonstrated pulsation. Venous blood also drained towards the On the basis of these findings, tortuousity rectus muscles (Fig:2), however venous and and wall thickness were chosen as photo­ arterial fields did not always coincide. graphic discriminants between arteries and Iris perfusion was similarily sectorial. veins:

arteries: tortuousity high; wall thickness > =

Discrimination Between Episcleral Arteries 2. veins: tortuousity low; wall thickness < = and Veins. 2. Angiographic Appearance (Figs. 2,4,5) In addition, arteries branched little and never Large, radial episcleral vessels were allocated showed laminar flow, whereas veins were to two categories, based upon their flow highly branched and 4 out of 8 revealed characteristics: streaming of blood. (I) Vessels that filled early in a perfusion field were highly fluorescent (> = 2 on Photographic Surveys (Fig. 6) analogue �cale) and had pulsatile flow. All the radial episc�ral vessels in each quad­ These were considered to be arteries. Sys- rant of 13 eyes (13 subjects) were classified as Fig. 2. Superior angiogram (magnification: 8mmlvertical field. timing: seconds after first flush) Top row: centrifugal filling of two adjacent anterior ciliary arteries, comprising a perfusion field. Second row: Single centrifugal anterior ciliary artery supplies adjacent perfusion field. This gives rise to episcleral arterial circle (�) which is fully perfused by 4 secs. Third row: centrifugal filling of the episcleral venous system. A superficial episcleral vein (0) is joined by an emissary vein (.). Fourth row: the late venous phase. This fades (20.0 secs), leaving beading of the fluorescein column in conjunctival vessels that perfuse inter­ . mittently. PA ITERNS OF BLOOD FLOW IN EPISCLERAL VESSELS 539 arteries or veins according to the above Direct, in which vessels joined end to side, or photographic criteria. In vessels that were end to end. not identifiable by major criteria (tortuousity and wall thickness) alone, the number of Indirect. their branches, and the characteristics of the The superimposition of conjuctival and vessels that flowed from or into them, were episcleral capillary beds made indirect com­ considered in addition. The mean incidence munication difficult to establish in most of arteries and veins over each muscle is illus­ angiograms. However it was confirmed in trated in Fig. 6. The incidence of arteries episcleral capillaries at the rectus muscle over the lateral rectus is lower than in the insertion in one intra-operative angiogram, other quadrants. Veips were concentrated in in which the conjunctiva had been retracted the vertical meridian, and eight out of 13 sub­ (Fig. 7). jects had no temporal vein. Direct (Fig. 5) Arteries The eac. was imaged in all 15 low power Direction of Blood Flow angiograms and ten of these demonstrated Forty radial arteries and 8 radial veins from direct arterial communications within it. 16 angiograms were adequately imaged for Arteries from different sources usually flow direction to be documented. joined at the site of a shared capillary bed. Twenty-five episcleral arteries flowed However, when merging vessels each away from the limbus: 15 carried blood supplied separate run-offs, the intervening towards the limbus. Arteries flowing in column of blood remained static, pulsating, opposing directions were found in nine out of and non-fluoresceinated. Fluorescence 21 angiographic fields (Fig. 7). spread gradually, presumably as a result of All veins drained away from the limbus diffusion of the dye. (Fig. 2). The circumstances giving rise to this sign were not often found. However, the eac. was demonstrated in this way in 3 angiograms; Scleral Perforators and the Episcleral Arterial communication between episcleral arteries Circle flowing away from the limbus and muscular Twenty-four arteries perforated the anterior arteries in 3 angiograms; and communication sclera in 16 angiograms. Two flowed back as 'between the eac. and a deep circulation (pre- anterior ciliary arteries, making no contribu­ sumed to be the intra-ocular arterial circle) tion to the eac; one fed the eac, but did not in one angiogram. give rise to an anterior ciliary artery: the remainder supplied both circulations. Capillaries (Fig. 4) The perforating arteries were classified In four of the 5 angiograms in which the con- according to their relationship to the eac: anterior (7), beneath (11), posterior (6). No single angiogram demonstrated arteries emerging from the sclera both anterior and posterior to the eac. Perforations were situated anterior to the eac. in both superior angiograms and posterior in both inferior studies. Their disposition was variable in the horizontal meridian.

Arterial Shunts Communications between arteries in the anterior segment fell into two categories: Indirect, in which two arteries shared a capil­ Fig. 3. Photograph of angiographic fi eld shown in lary bed. Fig. 2. 540 P. A. R. MEYER

Fig. 4. Left temporal videoangiogram (8mmlvertical fi eld; seconds after fi rst flush) Top row: filling of bifid anterior ciliary artery away fr om the limbus. Second row: fi lling of the episcleral arterial circle begins at 4 sec. and is complete at 8 sec. It supplies anterior can· junctiva and episclera. The posterior tarsal conjunctiva is supplied by a loop composed of two posterior tarsal arteries (�). Conjunctival capillaries derived fr om these and from the episcleral arterial circle communicate. Pulsation was seen between an anterior ciliary artery and muscular artery (p). junctival and episcleral capillary beds were episcleral contributions to arise as follows adequately imaged, episcleral capillaries (Fig. 8): arose from the eac and from branches of 1. Circumferential limbal that lie radial anterior ciliary arteries. In the remain­ anterior to the eac, draining radial conjuncti­ ing angiogram, episcleral detail was masked val capillaries and the limbal arcades. by the conjunctival capillary bed. 2. Veins that drain the episcleral capillary The anterior conjunctival capillaries filled net. from anterior roots of the eac, or equivalent 3. 4/8 of these veins received a deep contribu­ vessels arising directly from anterior ciliary tion. arteries. Veins that emerged from the sclera were distinguishable in stereo colour photographs Veins into two groups: fine, thin-walled vessels Eight radial episcleral veins could be fully that gradually surfaced as they flowed away characterised angiographically. They flowed from the limbus and large, thick-walled ves­ back towards a rectus muscle, accumulating sels that passed through distinct scleral episcleral branches. Photographs showed the foramina. Although only one of the latter PATTERNS OF BLOOD FLOW IN EPISCLERAL VESSELS 541

Fig. 5. Right temporial angiogram (8mmlvertical field; seconds after first flush) Filling emanates from a perforator (arrow). Note the pulsating dye fronts boardering non-perfused segments of perforating scleral artery (p) and episcleral arterial circle (c); (lOsec.). " Bottom row: (4mmlvertical field) illustrates a single cardiac cycle (arrows remain unchanged). was seen in the high-power studies, review of trated in Figure 9. Arterial flow was predo­ the low-power angiograms reveale

Superior An intraoperative angiogram over the lat­ eral rectus muscle is illustrated in Figure 7.

Discussion Fluorescein videoangiography is a powerful research technique with which to study the anterior segment circulations. Arteries and Nasal veins may now be distinguished by their flow characteristics, flow direction can be recorded, and flow velocity estimated. The results have resolved many paradoxes arising from previous work, and should rationalise the planning of anterior segment surgery.

The Arterial Rings of the Anterior Segment The anatomy of arterial communications in the anterior segment offers the potential for a network of shunts, in which the coronal arte­ rial circles (one within and one outside the

Inferior globe) are fed and joined by a saggittal arte­

Fig. 6. Mean incidence of arteries (clear) and veins rial ring (vs). (shaded) over each rectus muscle. The superficial (episcleral) arterial circle

(a) (b) Fig. 7. Intra-operative angiogram over lateral rectus muscle. (Conjunctiva has been retracted to expose only episcleral and muscular vessels). a.Arterial phase: Arrows show flow direction in anterior ciliary arteries. b. Capillary phase: Arrow indicates communication between anterior ciliary arteries through the episcleral capil­ lary bed. PATTERNS OF BLOOD FLOW IN EPISCLERAL VESSELS 543 has been confirmed. Anterior ciliary arteries commonly flow away from the limbus over all quandrants. Since only two long posterior ciliary arteries exist, both in the horizontal meridian,l. 5. 6 blood must be delivered to the superior and inferior anterior ciliary arteries by an intra-ocular arterial circle. In some angiograms direct communication between arteries was indicated during the flow phrase of the angiogram by columns of static, pulsating, non-fluorescent blood. This sign was discovered in a perforating anterior ciliary artery, and between anterior ciliary arteries and muscular arteries close to the rectus muscle insertion: it indicates two sites at which the muscular and long posterior ciliary contributions to the saggittal arterial ring do indeed meet. This sign requires each limb of a shunt to have a separate run-off, and one of these must lie within the angiographic field. These Fig. 8. Episcleral venous drainage. circumstances arose in only four out of 15 Arteries shaded, veins black. Arrows indicate ori­ angiograms. Although it indicates the exis­ gins of conjunctival arteries and veins. tance of saggittal arterial shunting, it does eac = episcleral arterial circle. not establish its incidence. ev = episcleral vein. 1. circumferential limbal veins (limbal venous cir­ Flow Dynamics in the Saggittal Arterial Ring cle). The direction of flow at any point within the 2. episcleral veins. saggittal arterial ring is presumably deter­ 3. perforating veins (presumed to be emissary veins mined by resistance within its component and veins draining the deep limbal microcircula­ tion). arteries and by the impedence of the circula­ tions that it supplies. These influences may be expected to vary under physiological and pathological conditions, or following surgery.

Fig. 9. Intra-operative angiograms over superior rectus muscles. (3 subjects) Arteries are black, veins shaded. Arrows indicate directions off/ow. 544 P. A. R. MEYER

In the angiograms upon which this study is late conjunctival and episcleral branches, based, most anterior ciliary arteries carried before passing back over the rectus muscles. blood away from the limbus, independent of This means that both arteries and veins the direction of gaze. Therefore normal sub­ emerge from foramina in the anterior sclera, jects derive the main blood supply to their and all carry blood in the same direction: anterior sclera and conjuctiva from within away from the limbus. However, they are the globe. distinguishable by their flow characteristics, The perfusion delays between adjacent enabling morphological differences to be episcleral fields presumably reflect the diffe­ deduced. rent routes taken by blood within the globe, Communication between superficial veins and confirms the proposal by Singh Hayreh in different fields was demonstrated photo­ and Scott9 that flow velocity in the intra-ocu­ graphically, and the failure of videoangiog­ lar arterial circle may be low. raphy to illustrate this probably reflects their The technique used for flow velocity esti­ numerous tributaries, their lower fluores­ mation required the indentification of a point cence intensity and the diffuse fluorescein on the advancing fluorescein front in two suc­ front that is found in the venous phase. cessive positions on the globe. The diffuse­ In colour photographic surveys, episcleral ness of this front (particularly in veins), veins were found to be concentrated in the uneven illumination (due to curvature of the vertical meridian: particularly over the globe) and auto- or pseudo-fluorescence all superior rectus muscle. combine to make this technique unreliable for absolute measurements, and more valu­ able for assessing variations in velocity within Conclusions for the Surgeon a single angiographic field. The anterior segment of the eye has evolved Since the anterior ciliary arteries form the a most elaborate matrix of arterial communi­ apex of an arterial ring, the large range of cations, perhaps in response to a requirement estimated systolic flow velocity within them is for constant perfusion pressure to the ciliary not surprising. apparatus. Despite this shunt system, squint Four out of five intra-operative angiog­ or detatchment surgery may sometimes give rams also demonstrated anterior ciliary rise to anterior segment ischaemia. arteries flowing away from the limbus. They During detachment surgery, the placement either met the muscular vessels to supply of a plomb or band may occlude a long post­ episcleral capillaries close to the rectus mus­ erior ciliary artery, breaking the saggittal cle insertion, or delivered blood into the arterial ring. Additional section of a muscu­ rectus muscles themselves. lar artery will give rise to anterior segment Intra-operative studies over the superior ischaemia if coronal shunting was inadequate rectus muscles illustrated the variability of or had been interfered with. flow dynamics at a single antomical site in Why transection of muscular arteries alone different subjects. However, further should cause anterior segment ischaemia is interpretation of these angiograms should be unclear, since this does not disturb the reserved, since the intra-ocular pressure was intraocular arterial supply to the iris and presumably low, the rectus muscles were ciliary body (the long posterior ciliary relaxed and the conjunctival vessing from the arteries and internal coronal arterial circle). episcleral arterial circle had been cut. It remains possible that the superficial limbs of the saggittal arterial ring are dominant in The Venous Drainage of the Anterior some SUbjects. Segment However, this study has confirmed that Venous drainage of the ciliary apparatus and emissary veins are a significant route for iris has been presumed to be through the drainage of the anterior segment, and they emissary veins or vortex veins2. This study leave the anterior episclera over the rectus confirmed the presence of the emissary veins muscles. There is evidence that the anterior which emerge from the sclera and accumu- segment ischaemia that may follow rectus PATTERNS OF BLOOD FLOW IN EPISCLERAL VESSELS 545 muscle surgery is the result of venous occlu­ venous and intra-ocular pressure must be vir­ sion (paper in preparation). tually equal in these pat.ients. Singh Hayreh and Scott 9 found that sector The destination of aqueous draining from iris perfusion defects followed section of the surgical fistulae is still a matter of con­ vertical, but not the horizontal, recti. They troversy, however episcleral veins have been attributed this to anterior ciliary artery occlu­ proposed.19 If this is correct, the impedence sion in sectors of the globe that received an of trans-scleral veins may determine the suc­ inadequate long posterior ciliary artery sup­ cess of these procedures. ply. The discovery that anterior ciliary Inflammatory disorders of the anterior scl­ arteries carry blood away from the limbus in era and cornea are associated with arterial both the vertical and horizontal meridians closure 14,20 and Meyer and Watson 8 prop­ requires reappraisal of this explanation. osed that interruption of flow in the Veins are concentrated in the vertical meri­ episcleral arterial circle may be responsible. dian, and venous occlusion may have However, if the anterior conjunctiva and accounted for the effects of vertical muscle episclera are normally supplied from within surgery in their patients. the globe, and arterial shunting can occur in When the ophthalmic surgeon cuts or the saggittal plane, closure of the intra-ocu­ cauterises vessels he diverts ocular blood lar arterial circle or scleral perforators must flow. The arterial communications of the also be considered. anterior segment appear to vary in incidence Anterior segment fluorescein videoangiog­ and calibre. When re-routing blood through raphy has proved to be a powerful method, them, it may be wise to follow the following yielding dynamic as well as morphological guidelines: data. It has shed new light upon the vagiaries (1) never interfere simultaneously with both of normal anterior segment blood flow, and it the deep and s:lperficial limbs of either sag­ is perhaps a matter of time before it becomes gittal arterial ring. a clinical investigative technique. (2) avoid disrupting both the saggittal and the coronal arterial circles. I would like to thank all the subjects who partici­ pated in this study, and Mr A.T. Moore and Mr. A. There is little evidence of effective venous Elliott who performed the dissections for the intra­ shunting in the anterior segment. Further­ operative angiograms. more, the distribution of anterior segment I am most grateful to Mr A. Quested and Mr A. veins is concentrated in the vertical meridian. Lacey (Medical Illustration Department, M.E.H., Therefore, City Road) who prepared the animations for the pre­ sentation upon which this paper is based. (3) if surgery is to involve one or both vertical This study was generously supported by the Iris rectus muscles, the adequacy of the remain­ Fund for the Prevention of Blindness. ing veins should be ensured. Paul Meyer is in receipt of a Welcome Research Fel­ It is hoped that the characterisation of lowship. these vessels in this paper will facilitate this. References This study has demonstrated communica­ 1 Leber T: Die Cirkulations- und Ernahrungs­ tion between the intra-ocular, and extra­ verhaltnisse des Auges. (Graefe-Saemisch ocular veins that drain the anterior segment: Handbuch der Gesamten Augenheilkunde.) the pressure within episcleral, conjuctival Leipzig: Engelmann, 1903,2: ch 1. and emissary veins must therefore be equal. 2 Kiss F: Der Blutkreislauf der Auges. Ophthal­ Intra-ocular veins remain patent only if their mologica 1943, 106: 225-50 intra-luminal pressure exceeds aqueous pres­ 3 Ashton N: Anatomical study of Schlemm's canal sure. Therefore the pressure within the and aqueous veins by means of Neoprene casts. Br. Ophthalmol. 291-303. episcleral venous system is equal to intra­ f. 1951,35: 4 Ashton N: Anatomical study of Schelmm's canal ocular pressure, less the gradient imposed by and aqueous veins by means of Neoprene the impedence of perforating veins. casts. Part II: aqueous 'veins.Br. f. Ophthal­ Although this impedence may vary consider­ mol. 1952,36: 265-7. ably, it must be low in the many subjects in 5 Ashton N and Smith R: Anatomical study of whom these vessels are large. Episcleral, Sch1emm's canal and aqueous veins by means 546 P. A. R. MEYER

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