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The Circulation of the Human Limbus

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Eye (1989) 3, 121-127 The Circulation of the Human Limbus PAUL A. R. MEYER Cambridge Summary The superficial circulations of the anterior segment of the human eye have been studied by the following techniques: photographic and video low-dose fluorescein angiography, video-microscopy using red-free light and stereoscopic colour pho­ tography. The results are combined to give a dynamic description of the Iimbal circulation, including its arterial supply and venous drainage. Limbal vessels we know more about the control of capillary In order to achieve optical clarity, blood growth here than at any other site in the body. vessels are excluded from the cornea in most Vascular invasion of cartilage is inhibited by species of mammal: this is possible because its a factor extractable from bovine aorta,8 metabolic activity is matched by the delivery thought to be chondroitin sulphate.9 This of glucose and. oxygen from aqueous and forms about 30 per cent of corneal pro­ tears.! However, the requirements of the cor­ teoglycan,! and the penetration of clear cor­ neo-scleral junction are substantially greater. nea by limbal capillaries may be suppressed in Corneal epithelium is largely renewed from the same way, although other hypotheses limbal stem cells,2.3 and there is evidence that have been proposed.lO the drainage of aqueous may be metabolically When placed within stromal pockets, demanding.4 tumour angiogenic factor,II,12 fibroblast These demands are met by an elaborate growth factor, 13 epidermal growth factor,n limbal capillary bed. The corneal epithelium catecholamines14 and prostaglandins (particu­ is supplied by a monolayer of superficial l)15. 6 arcades, and beneath these a receding bank of larly PGE 1 all stimulate limbal neo­ capillaries reaches down to the Canal of vascularisation. Hypoxia also appears to Schlemm. cause limbal vessels to proliferate, possibly as Capillaries of the limbus have thicker endo­ a result of the accumulation of ADP or lactic thelium and fewer fenestrations than those of acid. 17 This may account for the corneal vas­ the conjunctiva.5 They are anchored within cularisation that accompanies epithelial kera­ the corneal collagen matrix by a highly organ­ tinisation in vitamin A deficiency.IS ised adhesive of proteoglycan.6.7 Activated lymphocytes release angiogenic mediators,19 which may explain the neovascu­ Capillary growth and regression lar response to infection, corneal foreign This unusual circulation, much of which is bodies and grafts. This process is facilitated by imprisoned in collagen, might be considered granulocytes, 19.20 but not dependent upon unsuitable for studies of mediators affecting them. 21,22 vessel growth. However, the transparency of Therefore there is no single map of the lim­ the cornea has attracted many researchers and bal arcades. They form a cylindrical bank of Correspondence to: Paul A. R. Meyer, MRCP, Addenbrookes Hospital, Cambridge. 122 P. A. R. MEYER capillaries which may wax and wane according in the vertical meridian and the long posterior to environmental influences. ciliary arteries in the horizontal meridian.34 However, a recent study, in which emissary veins and anterior ciliary arteries were dis­ Vascular relationships tinguished by anterior segment fluorescein According to Leber's classical account,23 the videoangiography, has shown that, both in the anterior segment of the human eye has deep horizontal and vertical meridians, most and superficial circulations which both arise arteries and all veins do carry blood away from the ophthalmic artery: from the limbus.35 The circulations of the The long posterior ciliary arteries penetrate anterior ocular surface are therefore predomi­ the globe behind the equator, run forward nantly supplied from within the globe. within sclera, and cross the supra-choroidal The classical, static anatomical techniques space to join the major circle of the iris. This of indian ink injections33 and vascular cast­ intra-ocular arterial circle (which has recently ing36.37 do form the foundation for our know­ been shown to have an additional intra-mus­ ledge of the limbal vasculature.23.38.39 cular component24) supplies the iris and ciliary However, when circulatory dynamics are to apparatus. be described, there is no substitute for imag­ The anterior ciliary arteries-superficial, ing a living circulation using techniques such anterior continuations of the arteries to the as fluorescein angiography35.40 and video rectus muscles-were thought to supply the recording in red-free light. 41 limbus, anterior conjunctiva and episclera. In 1903 Leber was clear that the superficial Low dose anterior segment fluorescein and deep circulations were joined anteriorly angiography by substantial arteries that perforated the Retinal fluorescein angiography has been sclera and crossed the supra-choroidal space. practised since 1960,42 but extravasation of His findings have since been confirmed by 4 fluorescein has limited the value of anterior vascular castings,2 .25 but the direction of flow segment studies. However, by restricting the in these vessels has excited controversy. dose of fluorescein to prevent the saturation Whether studied by fluorescein angiogra­ of available ionic binding to circulating phy,26 or by the injection of radio-labelled albumin,43.44Ieakage from conjunctival capill­ microspheres,27 iris perfusion is found to aries may be reduced and resolution decline after section of the rectus muscles. enhanced.40 Low dose fluorescein angiograms This has been considered to indicate that the may be recorded photographically to give muscular/anterior ciliary arteries contribute high spatial resolution, or by video to achieve to the deep circulation.26.27 higher temporal resolution. Photographic fluorescein angiography of the anterior ciliary arteries themselves has yielded conflicting evidence. A number of Video recording in red-free light investigators have published angiographic The clinical use of red-free light to observe sequences in which anterior ciliary arteries blood flowin the anterior segment of the eye is appeared to fill away from the limbus.28.29.30 commonplace. However, this is difficult to Others have argued31.32 that these represent record by video since restriction of the band­ emissary veins, known to drain the deep cir­ width of illumination lowers light intensity, culations of the ciliary apparatus into the and most video cameras have enhanced sen­ superficial episcleral venous system. 33 sitivity to longer wavelengths. The technique Squint surgery upon the vertical, but not used for this study represents a compromise, the horizontal, rectus muscles may give rise tv in which a broad waveband of illumination perfusion defects in iris fluorescein angio­ below 600 nm is recorded by a CCD camera grams.34 This has prompted the suggestion which achieves peak sensitivity at 520 nm. that the circle of arteries in the iris root and This account of the limbal circulation con­ ciliary muscle (intra-ocular arterial circle) catenates the results of recent studies using may receive blood from the muscular arteries both techniques, paying particular regard to THE CIRCULAnON OF THE HUMAN LIMBUS 123 flow dynamics, arterial supply and venous normal subjects. Three hundred and sixty drainage. degree surveys were performed, with special reference to the changes in flow characteris­ Methods tics that accompany transit of blood through Photographic low dose fluorescein the limbal capillary bed and the anatomy of angiography venous drainage. The descriptions below are based upon find­ Illumination was by a 2S-watt incandescent ings in eight normal subjects, which have been lamp, filtered by a SOO-S80nm band-pass reported previously.40 Each volunteer interference filter. received one angiogram and colour photo­ Recordings were made on low-band graphs of the angiographic field. U-matic videotape using a COHU 4712 CCD Sodium fluorescein (120 mg) was injected camera. briskly into an ante-cubital fossa vein. The eye was illuminated at 1.S second intervals by 720 Results and Discussion Wsec flashesfrom an off-axis xenon flashunit, Delivery of Blood to the Anterior Segment mounted on a Zeiss photo-slit lamp. The (low-dose fluorescein videoangiography) exciting radiation was filtered by a 420- Using low-dose fluorescein videoangiogra­ 490 nm interference band pass filter; a long phy, arteries and veins may be distinguished pass filter (TSO = S1Snm) was placed in the by their flow characteristics and direction of imaging pathway. Photographs were taken flow can be recorded even when velocity is using the x 16 setting on the objective turret high. The velocity of an advancing fluorescein and a x2 magnifier (a magnification factor of front may be estimated, but this is not 3.S at the camera back). 400 ASA mono­ reliable. chrome film (Kodak Tri-X) was used, but was A study of 40 radial arteries from IS sub­ developed to 1200 ASA using Acuspeed jects demonstrated that more than 60% of developer (Patterson). anterior ciliary arteries filledfrom scleral per­ forations close to the limbus and flowed back Low dose fluorescein videoangiography towards the rectus muscles. They gave rise to These results are taken from studies of IS circumferential branches (the episcleral normal volunteers.35 The subjects received arterial circle) and radial vascular trunks, angiograms at low (13 mm/vertical screen) �ome of which met muscular arteries flowing and high (8 mm/vertical screen) magnifica­ in the opposite direction. This pattern of per­ tion, in addition
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