The Arterial Supply of the Eye of the Yak (Bos Grunniens)

中国科技论文在线 Research in Veterinary Science 84 (2008) 174–177 http://www.paper.edu.cn

The arterial supply of the eye of the yak (Bos Grunniens)

Bao-Ping Shao a, Yan-Ping Ding a, Shi-Yaun Yu b, Jian-Lin Wang a,*

a MOE Key Laboratory of Arid and Grassland Ecology, School of Life Sciences, Lanzhou University, Lanzhou, Gansu 730000, PR China b School of Life Sciences, Northwest Normal University, Lanzhou, Gansu 730070, PR China

Accepted 24 April 2007

Abstract

The heads and necks of 10 yaks were dissected to study the arterial supply to the eye of the yak in the Qinghai-Tibetan Plateau. The supply came from the internal ophthalmic, external eight ophthalmic, superficial temporal and malar arteries. The internal ophthalmic was one of sources of the posterior long ciliary artery. The external ophthalmic artery gave rise to branches to supply the dorsal oblique muscle and otherwise, and to take part in the formation of the ophthalmic rete mirabile. The ophthalmic rete mirabile gave off many branches to supply the rectus muscles of the eye and otherwise. The malar artery was one of the branches derived from the infraorbital artery, and its branches supplied the inferior, superior and third eyelids and otherwise. The superficial temporal artery detached off some branches to supply the lateral angle of the eye and otherwise, and anastomosed with the lacrimal artery of the ophthalmic rete mirabile. Ó 2007 Published by Elsevier Ltd.

Keywords: Yak; Eye; Arterial supply; Qinghai-Tibetan Plateau; Ophthalmic rete mirabile

1. Introduction mal, it is necessary to define the arterial supply to its eyes. Hideki et al. (2003) studied the blood supply to the retina The yak (Bos grunniens) is an important domestic ani- and the lens in the gerbil of both sexes from infancy to mal in some of the higher altitude areas of the world. It maturity. Wang (2002) studied the arterial supply to the was firstly domesticated about 4000 years ago in China eye of the Bactrian camel. Kanan (1972) observed the dis- where there are now more than 13 million yaks, making tribution of the external and internal ophthalmic arteries in up >90% of the world yak population. In the Qinghai- dromedary camel. Smuts and Bezuidenhout (1987) Tibetan Plateau, which is located about 3000–4700 m described some arteries that supply the eye of the drome- above sea level, the yaks provide a critical source of animal dary camel. Godinho and Getty (1975) described some products such as meat, milk and hides, etc. arteries that supply to the eye of the oxen. It is important to know the details of the arterial supply No reports describing the arterial supply to the eye in the of the eye of the yak to explore the morphological charac- yak have been published. The aim of the present study was teristics of the plateau animal. The eye is the visual organ to describe the origin, course and branches of the arteries of the vertebrate, the visual system is the most important that supply to the eye in the yak and to provide a morpho- sensory path, and approximately 80% of the outer informa- logical basis for further research on the adaptability of the tion enters brain through visual system. The yak can exist plateau animal, the comparative anatomy of the vertebrate in the Qinghai-Tibetan Plateau there is higher altitude and and the related clinical surgery of this domestic animal. less oxygen, the arterial supply of the eye plays an impor- tant role. So in studying the adaptability of the plateau ani- 2. Materials and methods

Abbreviation: A, arteria. Ten heads (cut above the second cervical vertebra) from * Corresponding author. Tel./fax: +86 931 8914075. adult yaks were collected from the Second Yak Slaughter- E-mail address: [email protected] (J.-L. Wang). house, Datong, Qinghai, China, after the animals had been

0034-5288/$ - see front matter Ó 2007 Published by Elsevier Ltd. doi:10.1016/j.rvsc.2007.04.019 转载 中国科技论文在线 http://www.paper.edu.cn

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killed by exsanguination for food. The specimens were fixed within 24 h of death by infusing them with 10% for- malin through the common carotid artery. After the spec- imens had been fixed for five to seven days, the specimens were then colored by injecting a solution of the red oils in ether (15:1) into the common carotid artery. All the animals were adults, but the sex and weight were not recorded. After again the specimens had been stored for one week, both sides of each specimen were carefully dissected to observe the origin, course, situations arrange- ments and branches of the arteries supply to the eye, fol- lowing the procedures described by Xie (1987), Li (1995) and Godinho and Getty (1975).

3. Results

The arterial supply of the eye of the yak came from the Fig. 2. Arterial blood supply to the right eye of the yak; lateral view. A. Supraorbital canal; B. Ethmoidal foramen and C. Optic nerve: (1) Carotid internal ophthalmic, external ophthalmic, superficial tem- artery; (3) External ophthalmic artery; (4) Ophthalmic rete mirabile; (5) poral and malar arteries. Supraorbital artery; (6) External ethmoidal artery; (7) Maxillary artery; (16) Posterior short ciliary artery; (17) Buccal artery; (18) Lacrimal artery. 3.1. Internal ophthalmic artery

The internal ophthalmic artery (Fig. 1) arose as a branch of the rete chiasmaticum. The artery left the rostral epidu- ral rete mirabile near the optic foramen and accompanied the optic nerve ventrally in the orbital fossa, where it joined with the branches of the external ophthalmic artery. The communicating branch was as a source of the posterior long ciliary artery (A. ciliaris longus posterioris lateralis).

3.2. External ophthalmic artery (A. ophthalmica externa)

The external ophthalmic artery (Figs. 1–3) arose from the dorsal wall of the maxillary artery following the origin Fig. 3. The deep arterial blood supply to the right eye of the yak; lateral of the buccal artery, at the level of the foramen orbitoro- view: (1) Carotid artery; (2) Superficial temporal artery; (3) External tundun (Fig. 1). It crossed the maxillary nerve laterally ophthalmic artery; (4) Ophthalmic rete mirabile; (5) Supraorbital artery; (6) External ethmoidal artery; (7) Maxillary artery; (8) Descending palatine artery; (9) Infraorbital artery; (10) Malar artery; (11) Third palpebral artery; (12) External ophthalmic artery; (13) Medial posterior long ciliary artery; (14) Medial superior palpebral artery; (15) Medial inferior palpebral artery; (28) Lateral inferior palpebral artery; (29) Lacrimal branch; (30) Lateral superior palpebral artery.

and entered the apex of the periorbita, where it gave off three branches, one entered the orbit with the ophthalmic nerve to form the ophthalmic rete mirabile, and the others took part in the formation of the rostral epidural rete (Figs. 1 and 2). From the ophthalmic rete mirabile arose to a common trunk for the supraorbital and external ethmoidal arteries (Figs. 1–3). After traversed the supraorbital canal, the supraorbital artery (A. supraorbitalis) do not gave off any branches in the orbit, and supplied the mucous mem- Fig. 1. Arterial blood supply to the right eye of the yak: medial view. D. brane of the frontal sinus and the musculature and skin lied Orbito-round foramen: (1) Carotid artery; (3) External ophthalmic artery; on the surface of the frontal bone directly (Figs. 1 and 2). (4) Ophthalmic rete mirabile; (5) Supraorbital artery; (7) Maxillary artery; (16) Posterior short ciliary artery; (18) Lacrimal artery; (19) Medial The external ethmoidal artery (A. ethmoidalis externa) was posterior long ciliary artery; (20) Central retinal artery; (21) Lateral the continuation of the external ophthalmic, which left the posterior long ciliary artery; (31) Internal ophthalmic artery. orbit through the ethmoidal foramen and entered the 中国科技论文在线 http://www.paper.edu.cn

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cranial cavity. It supplied the ethmoidal bone, the caudal along the medial side of the optic nerve entered the eyeball nasal septum and the dorsal nasal conha. The external eth- from the posterior half of the eyeball and successively moidal artery gave off a branch from its origin, which ran extended in the sclera and the epichoroid space towards dorsally and cranially entered the periorbit to supply the the limbus of cornea. There were three posterior short cil- ventral rectus muscle. At the medial surface of the sheath iary arteries (Fig. 1), which supplied the choroid. The cen- of the eye, one branch went rostrally and laterally along tral retinal artery (A. retina centralis)(Fig. 1) originated the medial border of the dorsal oblique muscle entered from the ophthalmic rete mirabile with the lateral posterior the conjunctival coat of the superior eyelid to supply the long ciliary artery or with the medial posterior long ciliary medial rectus and dorsal oblique muscles, the conjunctival artery, ventral to the optic nerve, and entered the optic surface of the superior eyelid and the fat body of the orbit. nerve to extend toward the cribriform area in the center of the nerve to supply the choroid. 3.3. Ophthalmic rete mirabile (rete mirabile ophthalmicum) 3.4. The malar artery (A. malaris) The ophthalmic rete mirabile was formed by the branches of the external ophthalmic artery (Figs. 1–3). A The malar artery (Fig. 1) was large and arose by a com- small part of the ophthalmic rete mirabile lay laterally to mon trunk with the infraorbital artery (A. infraorbitalis)in the original 85 art of the dorsal and lateral rectus muscles, the rostral part of the pterygopalatine fossa near the max- while the main part lay between the retractor oculi muscle illary foramen (Fig. 1). It passed dorsally and rostrally in and the ventral part of the dorsal rectus muscle. The oph- the orbital fossa to the medial angle of the eye and onto thalmic rete mirabile gave off some small muscular the lateral surface of the face to supply the eyeball and branches to supply the rectus, dorsal oblique and retractor its adnexa during its course it gave off three big branches oculi muscles, and the levator muscle of the superior eyelid. and some small branches. The formers were the third pal- The lacrimal artery was large and arose from the ophthal- pebral, medial superior palpebral and medial inferior mic rete mirabile (Figs. 2 and 3). After coursing to the lac- palpebral arteries (Fig. 3). The third palpebral artery rimal gland with the corresponding nerve along the rectus (A. palpebral tertiae) entered the periorbit of the eyeball, dorsalis, the lacrimal artery supplied the lacrimal gland. ran laterally and rostrally in the fat between the ventral Close to the lacrimal gland, the lacrimal artery gave off a and medial rectus muscles, penetrated the accessory lacri- branch to anastomose with the lacrimal branch of the mal gland, and then supplied the third eyelid. The medial superficial temporal artery. Shortly the lacrimal artery gave superior palpebral artery (A. palpebralis superior medialis) off two branches, the conjunctiva and anterior ciliary arter- went dorsally along the sheath of eyeball, the maxilla, the ies. The former coursed medially to the conjunctiva of the orbital surface of the lacrimal bone, and the medial surface superior eyelid and the latter supplied the dorsomedial of the origin of the ventral oblique muscle to supply the quadrant of the sclera. The lacrimal artery passed medio- cranial part of the superior eyelid, and to anastomose with ventrally from the ophthalmic rete mirabile and ran to the corresponding lateral artery of the superficial temporal the eyeball as a single vessel along the optic nerve. artery. The medial inferior palpebral artery (A. palpebralis After arising from the ophthalmic rete mirabile, medial inferior medialis) ran laterally among the sheath of the eye- to the ventral part of the dorsal rectus muscle, the external ball, the maxilla and the orbital surface of the zygomatic ophthalmic artery ran cranially and medially beneath the bone to supply the anterior part of the inferior eyelid and dorsal rectus muscle along the medial border of the retrac- to unite with the lateral artery of the superficial temporal tor oculis muscle, and entered the fibrous sheath of the artery. The latter supplied to the orbital fat, periorbita optic nerve at the optic foramen. Then it extended towards and mucous membrane of the maxillary sinus. the eyeball along the medial side of the optic nerve, and finally divided into the lateral and medial posterior long cil- 3.5. Superficial temporal artery (A. temporalis superficialis) iary, posterior short ciliary, central retinal arteries and some muscular branches to supply the retractor oculi mus- The superficial temporal artery (A. temporalis superficia- cle (Figs. 1 and 2). In some specimens, the lateral and med- lis)(Figs. 3 and 4) was the last branch of the external car- ial posterior long ciliary arteries originated from the otid in the region of the retroman dibular fossa, beyond ophthalmic rete mirebilie, and ran parallel to the medial which the latter continued as the maxillary artery (Figs. 3 side of the optic nerve towards the eyeball, where they uni- and 4). The superficial temporal artery ascended toward ted with each other. Having run from the ventral to the lat- the frontal region, after coursing under the parotid gland eral side of the optic nerve, the lateral posterior long ciliary and auricular muscles lateral to the temporomandibular artery (A. ciliaris longus posterioris lateralis) extended cra- joint on the lateral aspect of the zygomatic arch. It gave nially and laterally entered the eyeball from the posterior off the lateral superior palpebral and lateral inferior palpe- half of the eyeball and continued towards the border of bral arteries and lacrimal branch to the eye (Fig. 4). the cornea and the sclera. From the ophthalmic rete mira- The lateral superior palpebral artery (A. palpebralis supe- bile, the medial posterior long ciliary artery (A. ciliaris lon- rior lateralis) coursed caudal to the lateral angle of the gus posterioris medialis) also went cranially and medially eye and towards the superior eyelid. The lateral inferior 中国科技论文在线 http://www.paper.edu.cn

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as in the Bactrian camel (Wang, 2002). But the supraorbital artery did not give off any branches in the orbit, and directly traverses the supraorbital canal. The ophthalmic rete mirabile was only present in the yak, ox and buffalo (Godinho and Getty, 1975; Hunan, 1984), in which the formation, relationships and position are mostly the same as in cattle, but obviously difference between cattle and camel (Wang, 2002). There was no con- nection between the ophthalmic and epidural rete mirabiles in the yak. There were no obvious differences among the yak, ox, buffalo and Bactrian camel in the arteries that supplied Fig. 4. The superficial arterial supply to the left eye of the yak lateral view: the eyes, which came from the superficial temporal and (1) Carotid artery; (2) Superficial temporal artery; (22) Facial artery; (23) malar arteries (Godinho and Getty, 1975; Smuts and Bezu- Lingual artery; (24) Caudal auricular artery; (25) Transverse facial artery; idenhout, 1987; Hunan, 1984; Wang, 2002). However, the (26) Rostral auricular artery; (27) Cornual artery; (28) Lateral inferior facial, external ophthalmic and infraorbital arteries gave palpebral artery; (29) Lacrimal branch; (30) Lateral superior palpebral off some branches to supply the eye in the horse and don- artery. key (Xie, 1987).

palpebral artery (A. palpebralis inferior lateralis) was rela- Acknowledgements tively slender and arose caudal to the lateral angle of the eye. It ran toward the inferior eyelid. The lacrimal branch Authors are thankful to Dr. S.X. Li for his zealous help (Ramus lacrimalis) supplied to the lacrimal gland and anas- in collecting specimens. The study received financial sup- tomosed with towards the lacrimal artery of the ophthal- port from the National Natural Science Foundation of mic rete mirabile. China (39300097 and 30370163), and Open Foundation of Chinese Educational Department Key Laboratory of 4. Discussion Arid Agroecology.

The results of this study have shown that the arteries, References supplying the eye of the yak, were detached off from the internal ophthalmic, external ophthalmic, superficial tem- Godinho, H.P., Getty, R., 1975. The Anatomy of the Domestic Animals. poral and malar arteries, which were abundant and basi- fifth ed.. W.B. Saunders, London, Philadelphia, pp. 980–981. cally the same as in the ox and buffalo (Godinho and Hideki, L., Genzoh, I., Ei-ichi, M., 2003. Blood supply to the retina and the lens in the gerbil (Meriones unguiculatus). Anatomical Science Getty, 1975; Hunan, 1984). International 78, 36–41. The internal ophthalmic artery arose from the rete chi- Hunan, R.G., 1984. The Anatomy of the Chinese Water Buffalo. Hunan asmaticum, it left the rostral epidural rete mirabile near Scientific and Technology Press, Changsha, pp. 186–188. the optic foramen and accompanied the optic nerve ven- Kanan, C.V., 1972. Observations on the distribution of external and trally in the orbital fossa, where it joined with the branches internal ophthalmic arteries in the camel (Camelus dromedaries). Acta Anatomyca 81, 74–82. of the external ophthalmic artery, which were basically cor- Li, Y.L., 1995. Anatomy of the Dog. Science and Technology Press, responded with those of the ox, buffalo, horse and so on Shanxi, pp. 141–143. (Godinho and Getty, 1975; Hunan, 1984; Xie, 1987; Smuts Smuts, M.M.S., Bezuidenhout, A.J., 1987. Anatomy of the Dromedary. and Bezuidenhout, 1987). Clarendon Press, Oxford, pp. 155–156. The external ethmoidal artery of the yak detached off Wang, J.L., 2002. The Arterial supply to the eye of the bacterian camel (Camelas bactrianus). Veterinary Research Communication 26, 505– some branches to supply the ventral and medial dorsal rec- 512. tus oblique muscles, the conjunctiva of the superior eyelid Xie, Z.M., 1987. On the spot anatomy of donkey and horse. Agricultural and the fat body of the orbit, which were basically the same Press, Beijing, pp. 271–321.