Abstract
Rabbit and porcine corneas have been used in scientific research due to their structural similarity to the human cornea. Currently, there are no studies that have compared corneal collagen fibrillar diameter, interfibrillar distance and interlamellar distance between human and animal models. Ten pairs of porcine, rabbit, and human corneas were used. These were analysed using light and Transmission Electron microscopy. The collagen fibrillar diameter, interfibrillar distance and interlamellar distance were statistically compared between porcine, rabbit and human corneas. The human, porcine and rabbit; mean collagen fibrillar diameters were: 24.52 ± 2.09 nm; 32.87 ± 0.87 nm; and 33.67 ± 1.97 nm. The mean interfibrillar distances were: 46.10 ± 2.44 nm; 53.33 ± 2.24 nm; and 52.87 ± 2.73 nm, respectively. The collagen fibrillar diameter and interfibrillar distance of porcine and rabbit corneas were significantly different (p < 0.001) to the human corneal values but not form each other. The interlamellar distance of human, porcine and rabbit corneas was: 2190 ± 820 nm; 6460 ± 1180 nm; and 4410 ± 1330 nm, respectively. All the comparisons were statistically different, in porcine versus rabbit at the p < 0.01 level and both porcine and rabbit versus human at the p < 0.001 level. Histologically, all five layers (epithelium, Bowman's layer, stroma, Descemet membrane and endothelium) of the cornea were visible in all the three species. While neither animal model was structurally identical to the human cornea, they are both relatively close to being used as models to study the biomechanical effects of external insults/treatments to be extrapolated to the human cornea.
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References
Akhtar S, Almubrad T, Paladini I, Mencucci R (2013) Keratoconus corneal architecture after riboflavin/ultraviolet A cross-linking: ultrastructural studies. Mol Vis 19:1526–1537
Armitage WJ (2011) Preservation of human cornea. Transfus Med Hemoth 38(2):143–147
Bartholomew L, Pang D, Sam D, Cavender J (1997) Ultrasound biomicroscopy of globes from young adult pigs. Am J Vet Res 58(9):942–948
Brunette I, Rosolen SG, Carrier M, Abderrahman M, Nada O, Germain L et al (2011) Comparison of the pig and feline models for full thickness corneal transplantation. Vet Ophthalmol 14(6):365–377
Cafaro TA, Ortiz SG, Maldonado C, Espósito FA, Croxatto JO, Berra A et al (2009) The cornea of Guinea pig: structural and functional studies. Vet Ophthalmol 12(4):234–241
Cox JL, Farrell RA, Hart RW, Langham ME (1970) The transparency of the mammalian cornea. The Journal of Physiology 210(3):601–616
Davis FA (1929) The Anatomy and Histology of the Eye and Orbit of the Rabbit. Tr Am OphthSoc 27:400–441
Fernandez-Bueno I, Pastor JC, Gayoso MJ, Alcalde I, Garcia MT (2008) Muller and macrophage-like cell interactions in an organotypic culture of porcine neuroretina. Mol Vis 14:2148–2156
Ghosh F, Arnér K (2002) Transplantation of full-thickness retina in the normal porcine eye: surgical and morphologic aspects. Retina 22(4):478–486
Gyi TJ, Meek KM, Elliott GF (1988) Collagen interfibrillar distances in corneal stroma using synchrotron X-ray diffraction: a species study. Int J BiolMacromol 10(5):265–269
Hayashi S, Osawa T, Tohyama K (2002) Comparative observations on corneas, with special reference to bowman’s layer and descemet’s membrane in mammals and amphibians. J Morphol 254(3):247–258
Hayes S, Kamma-Lorger CS, Boote C, Young RD, Quantock AJ, Rost A et al (2013) The effect of riboflavin/UVA collagen cross-linking therapy on the structure and hydrodynamic behaviour of the ungulate and rabbit corneal stroma. PLoS ONE 8(1):e52860
Helena MC, Baerveldt F, Kim WJ, Wilson SE (1998) Keratocyte apoptosis after corneal surgery. Invest Ophth Vis Sci 39(2):276–283
Jay L, Brocas A, Singh K, Kieffer JC, Brunette I, Ozaki T (2008) Determination of porcine corneal layers with high spatial resolution by simultaneous second and third harmonic generation microscopy. Opt Express 16(21):16284
Kamma-Lorger CS, Boote C, Hayes S, Albon J, Boulton ME, Meek KM (2009) Collagen ultrastructural changes during stromal wound healing in organ cultured bovine corneas. Exp Eye Res 88(5):953–959
Lanchares E, Buey M, Cristóbal J, Lavilla L, Calvo B (2011) Biomechanical property analysis after corneal collagen cross-linking in relation to ultraviolet A irradiation time. Graefes Arch ClinExpOphthalmol 249(8):1223–1227
Majo F, Rochat A, Nicolas M, Jaoudé GA, Barrandon Y (2008) Oligopotent stem cells are distributed throughout the mammalian ocular surface. Nature 456(7219):250–254
Maurice DM (1957) The structure and transparency of the cornea. J Physiol 136(2):263–286
Nautscher N, Bauer A, Steffl M, Amselgruber WM (2016) Comparative morphological evaluation of domestic animal cornea. Vet Ophthalmol 19:297–304
Oh JY, In YS, Kim MK, Ko JH, Lee HJ, Shin KC et al (2007) Protective effect of uridine on cornea in a rabbit dry eye model. Invest Ophthalmol Vis Sci 48(3):1102–1109
Reid B, Song B, McCaig CD, Zhao M (2005) Wound healing in rat cornea: the role of electric currents. FASEB J 19(3):379–386
Rosolen SG, Saint-Macary G, Gautier V, LeGargasson JF (2001) Ocular fundus images with confocal scanning laser ophthalmoscopy in the dog, monkey and minipig. Vet Ophthalmol 4(1):41–45
Rosolen SG, Saint-Macary G, Gautier V, Le Gargasson JF (2002) SLO angiography: arterio-venous filling times in monkey and minipig. Vet Ophthalmol 5(1):19–22
Ruiz-Ederra J, García M, Hernández M, Urcola H, Hernández-Barbáchano E, Araiz J et al (2005) The pig eye as a novel model of glaucoma. Exp Eye Res 81(5):561–569
Seiler TG, Fischinger I, Senfft T, Schmidinger G, Seiler T (2014) Intrastromal application of riboflavin for corneal crosslinkingintrastromal application. Invest Ophthalmol Vis Sci 55(7):4261–4265
Sugiura T, Kurosaka D, Uezuki Y, Eguchi S, Obata H, Takahashi T (1999) Creating cataract in a pig eye. J Cataract Refract Surg 25(5):615–621
Wilson SE, Hong J-W (2000) Bowman’s layer structure and function: critical or dispensable to corneal function? A Hypothesis Cornea 19(4):417–420
Wilson SE, He Y-G, Weng J, Li Q, McDowall AW, Vital M et al (1996) Epithelial injury induces keratocyte apoptosis: hypothesized role for the interleukin-1 system in the modulation of corneal tissue organization and wound healing. Exp Eye Res 62(4):325–338
Wollensak G, Iomdina E (2009) Long-term biomechanical properties of rabbit cornea after photodynamic collagen crosslinking. ActaOphthalmol 87(1):48–51
Wollensak G, Spoerl E (2004) Collagen crosslinking of human and porcine sclera. J Cataract Refract Surg 30(3):689–695
Wollensak G, Spoerl E, Wilsch M, Seiler T (2004) Keratocyte apoptosis after corneal collagen cross-linking using riboflavin/UVA treatment. Cornea 23(1):43–49
Xiong C, Chen D, Liu J, Liu B, Li N, Zhou Y et al (2008) A rabbit dry eye model induced by topical medication of a preservative benzalkonium chloride. Invest Ophthalmol Vis Sci 49(5):1850–1856
Acknowledgements
Ari Samaranayaka ( Senior research fellow, Centre for Biostatistics, University of Otago, New Zealand) for assisting and approving the statistical analysis performed on this study.
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All authors contributed to the study conception and design. Conceptualization: SK.S, KC.O, LM, GJ.D. Methodology, formal analysis and investigation, writing—original draft preparation: SK.S, Writing—review and editing: KC.O, LM, GJ.D. Supervision: KC.O, LM, GJ.D.
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Subasinghe, S.K., Ogbuehi, K.C., Mitchell, L. et al. Animal model with structural similarity to human corneal collagen fibrillar arrangement. Anat Sci Int 96, 286–293 (2021). https://doi.org/10.1007/s12565-020-00590-8
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DOI: https://doi.org/10.1007/s12565-020-00590-8