Functional and microvascular anatomy of the ocular bulb in wild pig: a scanning electron microscopic study

This study searched the functional, macro- and microvascular anatomy of the ocular bulb in the 20 wild pigs to evaluate the effects of domestication on the eye comparatively by applying macroanatomical dissection techniques, Crossmon’s modified triple staining technique, and scanning electron microscopy (SEM) through corrosion cast technique. The ocular bulb was vascularized by the internal ophthalmic artery along with the external ophthalmic artery. Erythrocytes were observed in the capillaries of the inner layers of the retina. Distinctive functional adaptations were documented in the microvasculature of the ocular components, such as the marginal capillaries with irregular enlargements and narrowings following parallelly running and markedly convolute courses and ending with pinpoint-like terminations in the ciliary body. The iridal arterioles run a zigzag pathway, forming coherent undulations each other, and ending as bud-like structures, which seem to be artifacts due to incomplete filling of the resin. These peculiarities contribute probably to the compensation in capillary pressure.

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1. Onda E, Cioffi GA, Bacon DR, van Buskirk EM. Microvasculature of the human optic nerve. American Journal of Ophthalmology 1995; 120 (1): 92-102.
2. Krohn J, Bertelsen T. Corrosion casts of the suprachoroidal space and uveoscleral drainage routes in the human eye. Acta Ophthalmol Scand 1997; 75 (1): 32-35.
3. Okada S, Ohta Y. Microvascular pattern of the retina in the Japanese monkey (Macaca fuscata fuscata). Scanning Microscopy 1994; 8 (2): 415-427.
4. Ninomiya H, Inomata T. Functional microvascular anatomy of the horse eye: a scanning electron microscopic study of corrosion casts. Open Journal of Veterinary Medicine 2014; 4 (5): 91-101.
5. Ninomiya H, Inomata T. Microvascular anatomy of the pig eye: scanning electron microscopy of vascular corrosion casts. Journal of Veterinary Medical Science 2006; 68 (11): 1149- 1154.
6. Ninomiya H, Inomata T. Microvasculature of the hamster eye: scanning electron microscopy of vascular corrosion casts. Veterinary Ophthalmology 2005; 8 (1): 7-12.
7. Ninomiya H, Kuno H. Microvasculature of the rat eye: scanning electron microscopy of vascular corrosion casts. Veterinary Ophthalmology 2001; 4 (1): 55-59.
8. Ninomiya H, Inomata T, Kanemaki N. Microvascular architecture of the rabbit eye: a scanning electron microscopic study of vascular corrosion casts. Journal of Veterinary Medical Science 2008; 70 (9): 887-892.
9. Ninomiya H, Inomata T. Microvasculature of the mouse eye: scanning electron microscopy of vascular corrosion casts. Journal of Experimental Animal Science 2006; 43 (3): 149-59.
10. Morrison JC, DeFrank M, Van Buskirk EM. Comparative microvascular anatomy of mammalian ciliary processes. Investigative Ophthalmology & Visual Science 1987; 28 (8): 1325-1340.
11. Simoens P, Van den Broeck W, Lauwers H. Scanning electron microscopic study of the posterior ciliary veins in domestic ungulates. Folia Morphologica-Warszava-English Edition 2001; 60 (1): 21-26.
12. Aly K. Glycohitochemical, Immunohistochemical and Electron Microscopic Examination of the Bovine Eyeball: lmu. Munich, Germany: University Munich, 2003.
13. Yu D, Yu P, Balaratnasingam C, Cringle S, Su E, et al. Microscopic structure of the retina and vasculature in the human eye. Microscopy: Science, Technology, Applications and Education 2010: 867-875.
14. Bhutto IA, Amemiya T. Microvascular architecture of the rat choroid: corrosion cast study. The Anatomical Record 2001; 264 (1): 63-71.
15. Morrison JC, Fraunfelder F, Milne ST, Moore CG. Limbal microvasculature of the rat eye. Investigative Ophthalmology & Visual Science 1995; 36 (3): 751-756.
16. Morrison JC, Johnson EC, Cepurna WO, Funk RH. Microvasculature of the rat optic nerve head. Investigative Ophthalmology & Visual Science 1999; 40 (8): 1702-1709.
17. Sugiyama K, Gu Z-B, Kawase C, Yamamoto T, Kitazawa Y. Optic nerve and peripapillary choroidal microvasculature of the rat eye. Investigative Ophthalmology & Visual Science 1999; 40 (13): 3084-3090.
18. Prince JH, Diesem CD, Eglitis I, Ruskell G. Anatomy and histology of the eye and orbit in domestic animals. Anatomy and histology of the eye and orbit in domestic animals. 1960.
19. Bertschinger DR, Beknazar E, Simonutti M, Safran AB, Sahel JA, et al. A review of in vivo animal studies in retinal prosthesis research. Graefe’s Archive for Clinical and Experimental Ophthalmology 2008; 246 (11): 1505-1517.
20. Guduric-Fuchs J, Ringland LJ, Gu P, Dellett M, Archer DB, Cogliati T. Immunohistochemical study of pig retinal development. Mol Vis. 2009; 15: 1915-1928.
21. Kivell TL, Doyle SK, Madden RH, Mitchell TL, Sims EL. An interactive method for teaching anatomy of the human eye for medical students in ophthalmology clinical rotations. Anatomical sciences education 2009; 2 (4): 173-8.
22. Middleton S. Porcine ophthalmology. Veterinary Clinics of North America: Food Animal Practice 2010; 26 (3): 557-572.
23. Hodde K, Steeber D, Albrecht R. Advances in corrosion casting methods. Scanning microscopy. 1990; 4 (3): 693-704.
24. Minnich B, Lametschwandtner A. Scanning electron microscopy and vascular corrosion casting for the characterization of microvascular networks in human and animal tissues. Microscopy: Science, Technology, Applications and Education. 2010; 1: 29-39.
25. Verli FD, Rossi-Schneider TR, Schneider FL, Yurgel LS, de Souza MAL. Vascular corrosion casting technique steps. Scanning. 2007; 29 (3): 128-32.
26. Crossmon G. A modification of Mallory’s connective tissue stain with a discussion of the principles involved. The Anatomical Record. 1937; 69 (1): 33-38.
27. Denk H, Künzele H, Plenk H, Rüschoff J, Seller W. Romeis Mikroskopische Technik. 17., neubearbeitete Auflage. Urban und Schwarzenberg, München-Wien Baltimore. 1989; 1: 439- 450.
28. Morrison JC, DeFrank MP, Van Buskirk EM. Regional microvascular anatomy of the rabbit ciliary body. Investigative ophthalmology & visual science. 1987; 28 (8): 1314-1324.
29. Morrison JC, Van Buskirk EM. Ciliary process microvasculature of the primate eye. American journal of ophthalmology. 1984; 97 (3): 372-383.
30. Henkind P, De Oliveira LF. Retinal arteriolar annuli. Investigative ophthalmology & visual science. 1968; 7 (5): 584- 591.
31. Casellas D, Dupont M, Jover B, Mimran A. Scanning electron microscopic study of arterial cushions in rats: A novel application of the corrosion-replication technique. The Anatomical Record. 1982; 203 (3): 419-428.
32. Fourman J, Moffat D. The effect of intra-arterial cushions on plasma skimming in small arteries. The Journal of physiology. 1961;158 (2): 374-80.
33. Perkkiö J, Wurzinger L, Schmid-Schönbein H. Plasma and platelet skimming at T-junctions. Thrombosis research. 1987; 45 (5): 517-26.
34. Pannarale L, Onori P, Ripani M, Gaudio E. Precapillary patterns and perivascular cells in the retinal microvasculature. A scanning electron microscope study. Journal of anatomy. 1996; 188 (Pt 3): 693-703.
35. Ivanova E, Toychiev AH, Yee CW, Sagdullaev BT. Optimized protocol for retinal whole mount preparation for imaging and immunohistochemistry. Journal of visualized experiments: JoVE. 2013; (82): e51018.
36. Rootman J. Vascular system of the optic nerve head and retina in the pig. The British journal of ophthalmology. 1971; 55 (12): 808-819.
37. Campbell J, Zhang M, Hwang T, Bailey S, Wilson D, et al. Detailed vascular anatomy of the human retina by projectionresolved optical coherence tomography angiography. Scientific reports. 2017; 7: 4220.