Vascular corrosion casts of 12 equine, 15 bovine and 50 porcine eyes were studied scanning electron microscopically for the presence of posterior ciliary veins. These veins drain a postequatorial segment of the choroid and emerge near the posterior bulbar pole. They complement the four vorticose veins that emerge near or at the equatorial zone of the eyeball and the slender choroidoretinal veins that drain the peridiscal area of the choroid. Posterior ciliary veins were observed in all equine and bovine eyes examined. In these species they presented a large variation in size, number and position. In contrast, posterior ciliary veins were only present in two porcine eyes where they were represented by one and two vessels, respectively. The morphology and variability of these vessels is illustrated and their nomenclature and functional significance are discussed

Broeck, Wim Van den

Lauwers, Henri

Simoens, Paul

English

Via Medica Journals

Folia Morphol. Vol. 60, No. 1, pp. 2126Copyright ' 2001 Via MedicaISSN 00155659www.fm.viamedica.plO R I G I N A L  A R T I C L E21Scanning electron microscopic study of theposterior ciliary veins in domestic ungulatesPaul Simoens, Wim Van den Broeck, Henri LauwersDepartment of Morphology, Faculty of Veterinary Medicine, Ghent University, Belgium[Received 16 October 2000; Accepted 23 November 2000]Vascular corrosion casts of 12 equine, 15 bovine and 50 porcine eyes werestudied scanning electron microscopically for the presence of posterior ciliaryveins. These veins drain a postequatorial segment of the choroid and emergenear the posterior bulbar pole. They complement the four vorticose veins thatemerge near or at the equatorial zone of the eyeball and the slender choroidoret-inal veins that drain the peridiscal area of the choroid. Posterior ciliary veins wereobserved in all equine and bovine eyes examined. In these species they presenteda large variation in size, number and position. In contrast, posterior ciliary veinswere only present in two porcine eyes where they were represented by one andtwo vessels, respectively. The morphology and variability of these vessels is illus-trated and their nomenclature and functional significance are discussed.key words: ophthalmology, angiology, veins, choroid, horse, ox, pigINTRODUCTIONThe venous outflow of the choroid in domestic ani-mals is mainly provided by the four vorticose veinsthat emerge near or at the equatorial area of theeyeball. The morphology of these veins has beendescribed in detail for all domesticated mammalianspecies including herbivores [1,9], carnivores [4,10]and pigs [6]. The vorticose veins are complementedby much smaller veins that drain the peridiscal seg-ments of the choroid and leave the eyeball near theposterior bulbar pole, where they anastomose withthe retinal venules. These peridiscally emerging veinshave been designated by various names such as shortposterior ciliary veins [4], cilioretinal veins [2] andchoroidoretinal veins [6]. The latter term will be usedfurther below in this text, because of its conformityto the nomenclatory rules defined by official veteri-nary anatomical nomenclature [5,6]. These chor-oidoretinal veins are most obvious in the dog [4] andcat [10], and have also been observed in the porcineeye [6]. In contrast, they have not been described inelaborate classic studies on the equine [1] and bo-Address for correspondence: Paul Simoens, Department of Morphology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133,9820 Merelbeke, Belgium, tel: + 32 9 264 77 12, fax: + 32 9 264 77 90, e-mail: Paul.Simoens@rug.ac.bevine [9] ocular vasculature, and neither are theymentioned in recent anatomical and ophthalmologicliterature dealing with these species. However, theancient anatomical study of the equine eye by Bach[1] contains an illustration showing a large innomi-nate vein which emerges far posterior to the vorti-cose veins but is too far remote from the optic discarea to be considered as a choroidoretinal vein. Toour knowledge the presence of such a particular ves-sel, which is apparently complementary to the vorti-cose and choroidoretinal veins, has not been con-firmed afterwards in veterinary literature. Thereforethe present study was performed in order to gatherinformation about the presence and the character-istics of these vessels, which will be further referredto by the name posterior ciliary veins.MATERIAL AND METHODSThis scanning electron microscopic (SEM) study wasperformed on vascular corrosion casts of 12 equine,15 bovine and 50 porcine eyes. The animals were ofvarious breeds and ages, and were subjected to eu-22Folia Morphol., 2001, Vol. 60, No. 1thanasia for reasons other than ocular disease. Im-mediately after death they were exsanguinated andthe cranial blood vessels were flushed with a salinesolution through a catheter inserted in the maxillaryarteries (horses) or the common carotid arteries (oxenand pigs). Subsequently the orbital vasculature wasfilled by the same approach with pigmented meth-ylmethacrylate (Batsons No. 17, Polysciences Ltd.,St Goar, Germany). After polymerisation for 8 h, theorbital contents were macerated by immersion ina 25% solution of potassium hydroxide at room tem-perature during 72 h, whereafter the corrosion castswere rinsed in water and air-dried. Peribulbar bloodvessel casts were dissected for exposing the choroi-dal vasculature under a Wild M7A stereomicroscope(Heerbrugg, Switzerland). The bulbar casts weremounted with double-sided adhesive tape on alu-minium stubs, sputter-coated with platinum (AutoFine Coater JFC-1300 JEOL, Tokyo, Japan) and exam-ined by means of a JEOL JSM 5600 LV (Tokyo, Japan)scanning electron microscope in high vacuum modeat 10 kV.RESULTSPosterior ciliary veins were present in all equine andbovine eyes but were inconstant in the porcine eyes.They collected a variable amount of postequatorialchoroidal veins that were located in the watershedzones between the vorticose veins and emergedpostequatorially through the sclera (Fig. 1). The size,number and position of these veins were subject toconsiderable variation.In horses, the number of posterior ciliary veinsranged from one single branch to as many as 9 slen-der veins which emerged separately, with an aver-age number of 5 veins per eye. The luminal diam-eter of the veins measured on vascular casts variedfrom less than 0.1 mm to 0.5 mm. One or more pos-terior ciliary veins were always observed in the dor-sal watershed zone between the dorsomedial anddorsolateral vorticose veins (Figs. 25). These con-stant but variably shaped veins drained territoriesthat were supplied by the corresponding dorsal pos-terior ciliary artery. In seven horses, one or two ven-tral posterior ciliary veins were located in the ventralwatershed zone, i.e. between the ventromedial andventrolateral vorticose veins. These slender veinsdrained a rather small peridiscal choroidal area sup-plied by the ventral posterior ciliary artery and thechoroidoretinal arteries (Fig. 6). Additional posteriorciliary veins were observed in the lateral watershedzones between the dorso- and ventrolateral vorti-cose veins in five eyes, and in the medial watershedzone between the dorso- and ventromedial vorticoseveins in four eyes. These lateral and medial posteriorciliary veins were slender and emerged near thebranches of the short posterior ciliary arteries enter-ing the choroid (Fig. 7).A similar distribution of posterior ciliary veins wasobserved in the bovine eyes. One or more veins werepresent in the dorsal, ventral and horizontal water-shed zones between the vorticose veins in each eye-ball. They varied in number and size, ranging froma single vessel with a diameter of more than 1 mm(Figs. 89) to several slender veins emerging betweenthe ramifying or coiled branches of the short poste-rior ciliary arteries (Figs. 1011). After piercing thesclera, most of these vessels discharged as separateveins into the ophthalmic venous plexus (Figs. 89A),but in one particular case the emerging vein curvedanteriorly and anastomosed with the retrobulbarstem of the dorsolateral vorticose vein (Fig. 9B).In contrast to the equine and bovine eyes, poste-rior ciliary veins were inconstant in the porcine eyes.They were observed only in two out of 50 eyes. TheFigure 1. Compilation drawing based on 10 equine eyes illustrat-ing the position of the posterior ciliary veins (small circles) emerg-ing from the choroid in the watershed zones between the vorticoseveins. This schematic caudal view of the left eye shows the con-tours of the eyeball (outer border line), the choroid (shaded innerborder line) and the optic disc (asterisk). Particular posterior ciliaryveins that are identified by numbers (27) are illustrated in thenext figures bearing the same numbers; a  lateral long posteriorciliary artery; b  lateral short posterior ciliary arteries; c  me-dial long posterior ciliary artery; d  medial short posterior ciliaryarteries; e  dorsal posterior ciliary artery; f  ventral posteriorciliary artery; g  choroidoretinal arteries; DL  dorsolateral vor-ticose vein; DM  dorsomedial vorticose vein; VL  ventrolateralvorticose vein; VM  ventromedial vorticose vein.23Paul Simoens et al., Posterior ciliary veins in ungulatesFigure 4. Double-branched posterior ciliary vein (V) emerging from thedorsal watershed zone in an equine eye. Arrows indicate choroidal ar-teries crossing over some of the venous branches. Scale bar = 1 mm.Figure 2. Caudal view of an equine choroidal vascular cast showingone relatively large (asterisk) and several slender posterior ciliaryveins (arrows) emerging from the watershed zone between the dor-solateral choroidal veins (to the left) and the dorsomedial choroidalveins (to the right). Notice the close association between the poste-rior ciliary veins and the branches of the dorsal posterior ciliary ar-tery (painted in red) entering this area. Scale bar = 1 mm.Figure 3. Single posterior ciliary vein (V) emerging from the dorsalwatershed zone in an equine eye in close association with a poste-rior ciliary artery (A) entering the same area. Scale bar = 1 mm.Figure 5. Posterior pole area of an equine choroidal vascular castpresenting a posterior ciliary vein (V) surrounded by coiled choroi-dal arterial branches (arrows) given off by a choroidoretinal arterythat has been removed in order to expose the flattened intra- andextrascleral segments of the vein (asterisk). Scale bar = 1 mm.first case was a 7-month-old Vietnamese miniaturepig with a 0.2 mm wide vein which left the choroid2 mm ventrolateral to the optic disc margin, piercedthe sclera and discharged into a choroidoretinal veinafter collecting a slender episcleral vein (Fig. 12). Theother case was a 1-month-old Belgian landrace pig-let having a similar dorsal posterior ciliary vein and amuch smaller ventral counterpart vein, which bothemerged from the peridiscal area of the choroid anddischarged into the choroidoretinal veins.DISCUSSIONThis study demonstrates that the ocular vascular tu-nic of large domestic animals contains particularchoroidal veins that emerge postequatorially fromthe eyeball and are complementary to the vorticoseand choroidoretinal veins. The existence of thesevessels was suggested more than a century ago inan illustration of the equine eye [1], but has not been24Folia Morphol., 2001, Vol. 60, No. 1Figure 6. Large posterior ciliary vein (V) emerging from the equine choroid ventral to the optic disc border (asterisk) and draining a choroidalsegment supplied by the ventral posterior ciliary artery (1) and branches of choroidoretinal arteries (2). Scale bar = 1 mm.Figure 7. Posterior ciliary vein (V) emerging caudally from the lat-eral watershed zone of the equine choroid. The vein stem is sur-rounded by several arterial branches (asterisks) of a lateral shortposterior ciliary artery that has been cut for better exposure of thevein. Scale bar = 1 mm.Figure 8. Lateral stereomicroscopic view of the choroidal vascularcast of a left bovine eye showing a large posterior ciliary vein (1)emerging from the dorsal watershed zone between the dorsolater-al (2) and dorsomedial (3) vorticose veins. Other blood vessels la-belled are the ventrolateral (4) and ventromedial (5) vorticose veinsas well as the lateral (6) and medial (7) long posterior ciliary arter-ies which arise from the major bulbar artery, i.e. the anastomoticbranch between the external and internal ophthalmic arteries (8).Scale bar = 5 mm.documented since. In the present study, however,such veins were observed in all eyes of horses andoxen that were examined, as well as in a minority ofthe porcine eyes. In contrast, the authors could findno evidence for the presence of such vessels in fe-line and canine eyes neither by reviewing the litera-ture reports nor by studying a high number of vas-cular corrosion casts from these species. The fact thatthese veins were constantly present in the largeequine and bovine eyeballs suggests that they fulfila functional demand by providing an additional out-flow route for the high volume of choroidal blood inthese species. Such a function is fully in line with theobservation that these vessels are positioned in be-tween the vorticose and choroidoretinal veins andform numerous anastomoses with both sets of veins.25Paul Simoens et al., Posterior ciliary veins in ungulatesFigure 9. A) Dorsal stereomicroscopic view of the posterior ciliary vein (1) of the vascular cast of the left bovine eye illustrated in Fig. 8,showing the separate extrabulbar course of the emerging posterior ciliary vein (arrows). Same legend as in Fig. 8; Scale bar = 5 mm.B) Dorsal stereomicroscopic view of the vascular cast of a right bovine eye showing a posterior ciliary vein (1) which emerges from the samearea as in Fig. 9A but bends anteriorly (arrows) after leaving the eyeball to join the extrabulbar stem of the dorsolateral vorticose vein (2).Figure 10. Large posterior ciliary vein (V) emerging from the dorsalwatershed zone in a choroidal vascular cast of a bovine eye. Ob-serve the numerous coiled arterial clusters of short posterior ciliaryarteries (A) entering the same area. Scale bar = 1 mm.Figure 11. Postequatorial segment of the medial watershed zonein a choroidal vascular cast of a bovine eye showing a posteriorciliary vein (V) emerging caudal and parallel to a short posteriorciliary artery (A). Scale bar = 1 mm.The iconographic documentation of the post-equatorially emerging choroidal veins clearly illus-trates that the size, number and position of thesevessels are subject to considerable variation. Despitethis variability, however, the high frequency of theseveins indicates that they might be functionally andclinically important for draining the blood from thechoroid. Because of their location in the choroidalwatershed zones, i.e. between adjacent vorticoseveins or between the vorticose and choroidoretinalBA26Folia Morphol., 2001, Vol. 60, No. 1Figure 12. Choroidal vascular cast of a Vietnamese miniature pigshowing a posterior ciliary vein (V) which emerges 2 mm ventralto the optic disc margin (asterisk). The extrascleral segment of thevein (arrowheads), which is incompletely filled with casting medi-um, receives an episcleral vein (arrow). A short posterior ciliaryartery (A) enters and ramifies in the adjacent peridiscal area of thechoroid. Scale bar = 1 mm.veins, the posterior ciliary veins provide anastomot-ic pathways for shunting blood towards ischaemicchoroidal areas in cases of vascular occlusion. Theimportance of such venous anastomoses betweenthe various choroidal segments has been demonstrat-ed in experimental animal studies [7] as well as inhuman patients [3].No proper terminology for the postequatoriallyemerging choroidal veins has been found in the fewmorphologic papers describing bulbar angiology indomestic animals [1] nor in official veterinary ana-tomical nomenclature [5]. Yet it is recommended tohave a specific name for these vessels because oftheir frequency and their functional potential. Inconformity with the proposal for designating thecorresponding arteries as posterior ciliary arteries[8], we suggest designating these particular veins asVv. ciliares posteriores. This terminology would onlyrequire a minor adaptation of the official anatomi-cal nomenclature [5] which actually contains onlythe less specific term Vv. ciliares. By adding distin-guishing adjectives to this term it would be possibleto differentiate between the Vv. ciliares anteriores,which drain the anterior ocular segments includingthe scleral venous plexus, and the Vv. ciliares pos-teriores, which emerge postequatorially from theeyeball. The introduction of these separate terms isin line with the official nomenclature used for thecorresponding arteries [5] and is recommended inview of the different functional and clinical signifi-cance of both types of veins.ACKNOWLEDGEMENTSThe technical assistance by Mr R. De Moor and B. DePauw and the financial support by the Research Fundof Ghent University (BOF Grant 011B7597) are thank-fully acknowledged.REFERENCES1. Bach L (1894) Ueber die Gefässe des Pferdeauges mitbesonderer Berücksichtigung der Gefässversorgung derAderhaut. Arch wissenschaft prakt Thierheilkunde, 20:241256.2. Brooks DE, Samuelson DA, Gelatt KN, Smith PJ (1989)Scanning electron microscopy of corrosion casts of theoptic nerve microcirculation in dogs. Am J Vet Res, 50:908914.3. De Laey JJ (1977) Fluoroangiografische studie van denormale en pathologische chorioidea bij de mens. JunkW Publishers, Den Haag.4. Hetkamp D (1972) Korrosionsanatomische Untersuchun-gen der Blutgefäbe des Auges des Haushundes (Canisfamiliaris L.) unter besonderer Berücksichtigung des Kap-illarsystems. Thesis, Justus Liebig-Universität Giessen.5. Nomina Anatomica Veterinaria (1994) 4th edition,World Association of Veterinary Anatomists, Zurich.6. Simoens P (1985) Morphologic study of the vasculatureof the orbit and eyeball of the pig. PhD thesis, Ghent.7. Simoens P (1993). In vivo en in vitro studie van expe-rimentele occlusie van chorioidale en retinale bloed-vaten bij het miniatuurvarken. Verhand Kon Acad Ge-neesk Belgiº, 4: 319375.8. Simoens P, Muylle S, Lauwers H (1996) Anatomy of theocular arteries in the horse. Equine Vet J, 28: 360367.9. Smith P (1921) On the eye of the ox and its internalblood vessels. British J Ophthalmol, 5: 385410.10. Wong VG, Macri FJ (1964) Vasculature of the cat eye.Arch Ophthalmol, 72: 351358.

Scanning electron microscopic study of the posterior ciliary veins in domestic ungulates

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Scanning electron microscopic study of the posterior ciliary veins in domestic ungulates

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