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Scanning electron microscopy study of the tarsal and orbital conjunctival surfaces compared to peripheral corneal epithelium in pigmented rabbits

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Abstract

The mammalian palpebral conjunctiva has not been systematically evaluated by scanning electron microscopy (SEM). The upper eyelid of female grey rabbits (2 kg) was fixed in its extended conformation at 15.00 h; some corneas were prepared with the same fixative protocol. The corneal epithelium, within 1 mm of the limbus, is a mosaic of small-to-large (average cell area of 693 m2) squamous cells with light, medium or dark appearance due to different densities of cell surface microplicae. The tarsal conjunctiva was a 1.5 to 3 mm wide mosaic of small (average cell area of 86 μm2) non-desquamating polygonal cells having distinctive light and dark appearances due surface microplicae. The orbital portion of the palpebral conjunctiva is also composed of small (average cell area of 87 μm2) non-desquamating polygonal cells but with a uniform medium-grey appearance due to a relatively consistent density of surface microvilli. Several types of intercellular pore-like openings were also present across the palpebral surface but not the corneal epithelial surface. Very small type 1 pores (1.5 to 5 μm diameter) were present at a density of 480 to 760/mm2 for the tarsal and 80–160/mm2 for orbital conjunctiva. Slightly larger (2.5 to 18 μm diameter) type 2 pores with distinct borders were present at 120–200/mm2 across the orbital conjunctiva. Very large (10–109 μm diameter) type 3 (Henle) pores were present at 40 to 280/mm2 especially at the tarsal/orbital transition zone. Type 4 pores (goblet cell orifices) were oval with a peripheral ring of microvilli and were present at 40 to 160/mm2 for tarsal and 800 to 1600/mm2 for orbital conjunctiva. The rabbit palpebral conjunctival surface is thus distinctly different from the peripheral corneal epithelium across which it slides following eyelid closure.

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References

  1. Duke-Elder S, Wybar KC. The eyelids. In: System of ophthalmology. Vol. II. The anatomy of the visual system. CV Mosby, St. Louis, MO. 1962; pp. 507

    Google Scholar 

  2. Duane, A. Protective organs (adnexa) of the eye. In: Fuch's textbook of ophthalmology. JB Lippincott, Philadelphia, PA. 1924; pp: 4

    Google Scholar 

  3. Bremer JL. A Textbook of Histology. Blakiston Co., Philadelphia, PA. 1944; pp. 644

    Google Scholar 

  4. Prince JH, Diesser, CD, Eglitis I, Ruskell GL. Anatomy and Histology of the Eye and Orbit in Domestic Animals. Charles C Thomas, Springfield, IL. 1960; pp. 154

    Google Scholar 

  5. Eglitis I. The glands. In: Prince JH (ed) The Rabbit in Eye Research. Charles C Thomas, Springfield, IL, 1964; pp. 33–37

    Google Scholar 

  6. DiFiore MSH. Atlas of Human Histology. Lea & Feibiger, Philadelphia, PA. 1961; pp. 201

    Google Scholar 

  7. Wolff E. The anatomy of the eye and orbit. HK Lewis & Co. Ltd., London. 1976; pp. 187

    Google Scholar 

  8. Spooner JD. Ocular Anatomy. Butterworths, Boston. 1976; pp. 92

    Google Scholar 

  9. Blogg JR. The eye in veterinary practice. Extraocular disease. Volume 1. WB Saunders Co, Philadelphia. 1980; pp. 349

    Google Scholar 

  10. Jakobiec FA, Iwamoto, T. Ocular adnexa—introduction to lids, conjunctiva and orbit. In: Jakobiec FA (ed) Ocular anatomy, embryology, and teratology. Harper & Row Publ., Philadelphia. 1982; pp. 677–731

    Google Scholar 

  11. Ruskell GL. The conjunctiva. In: Bennett ES, Weissman BA (eds) Clinical Contact Lens Practice. Philadelphia, JB Lippincott. Chapter 3. 1991.

    Google Scholar 

  12. Rohen JW. Zur funktionellen Morphologie der Conjunctiva. Fortschr Ophthalmol. 1986; 83: 13–24.

    PubMed  CAS  Google Scholar 

  13. Pfister RR. The normal surface of conjunctiva epithelium. A scanning electron microscopic study. Invest Ophthalmol 1975; 12: 267–279

    Google Scholar 

  14. Honegger H, Brewitt H. Das normal Hornhaut und Bindehautepithel im rasterelektronen-mikroskopischen Bild. Ber Dtsch Ophthalmol Ges 1978; 75: 646–648

    Google Scholar 

  15. Pfister RR, Renner ME. The corneal and conjunctival surface in vitamin A deficiency—a scanning electron microscope study. Invest Ophthalmol Vis Sci 1978; 17: 874–883

    PubMed  CAS  Google Scholar 

  16. Latovic S. The ultrastructure of normal conjunctival epithelium of the guinea pig. IV. The palpebral and perimarginal zones. Acta Ophthalmol 1979; 57: 321–335

    Google Scholar 

  17. Basrur PK, Basu PK. Effect of cigarette smoke on the surface structure of the conjunctival epithelium. Can J Ophthalmol 1980; 15: 20–23

    PubMed  CAS  Google Scholar 

  18. Weyrauch KD. The surface of the conjunctiva in domestic ruminants. A scanning electron microscopic investigation. Acta Anat. 1984; 119: 27–32

    Article  PubMed  CAS  Google Scholar 

  19. Steuhl K-P. Ultrastructure of the conjunctival epithelium. Dev Ophthalmol 1989; 19: 1–106

    PubMed  CAS  Google Scholar 

  20. Schramm U, Unger K, Keeler C. Functional morphology of the nictitating membrane in the domestic cat. Annals Anat. 1994; 176: 101–108

    CAS  Google Scholar 

  21. Greiner JV, Leahy CD, Welter DA, Hearn SL, Weidman TA, Korb DR. Histopathology of the ocular surface after eye rubbing. Cornea 1997; 16: 327–332

    Article  PubMed  CAS  Google Scholar 

  22. Greiner JV, Covington HI, Allansmith MR. Surface morphology of the human upper tarsal conjunctiva. Am J Ophthalmol 1977; 83: 892–905

    PubMed  CAS  Google Scholar 

  23. Greiner JV, Covington HI, Allansmith MR. Surface morphology of giant papillary conjunctivitis in contact lens wearers. Am J Ophthalmol 1978; 85: 242–252

    PubMed  CAS  Google Scholar 

  24. Greiner JV, Covington HI, Korb DR, Allansmith MR. Conjunctiva in asymptomatic contact lens wearers. Am J Ophthalmol 1978; 86: 403–413

    PubMed  CAS  Google Scholar 

  25. Greiner JV, Henriquez AS, Covington HI, Weidman TA, Allansmith MR. Goblet cells of the human conjunctiva. Arch Ophthalmol 1981; 99: 2190–2197

    PubMed  CAS  Google Scholar 

  26. Greiner JV, Allansmith MR. Effect of contact lens wear on the conjunctival mucous system. Ophthalmology 1981; 88: 821–832

    PubMed  CAS  Google Scholar 

  27. Greiner JV, Covington HI, Fowler SA, Weidman TA, Allansmith MR. Cell surface variations of the human upper tarsal conjunctiva. Ann Ophthalmol 1982; 14: 288–290

    PubMed  CAS  Google Scholar 

  28. Dark AJ, Durrant TE, McGinty F, Shortland JR. Tarsal conjunctiva of the upper eyelid. Am J Ophthalmol 1974; 77: 555–564

    PubMed  CAS  Google Scholar 

  29. Dilly PN, Mackie IA. Surface changes in the aneasthetic conjunctiva in man with special reference to the production of mucus from a non-goblet cell source. Br J Ophthalmol 1981; 65: 833–842

    PubMed  CAS  Google Scholar 

  30. Greiner JV, Gladstone L, Covington HI, Korb DR, Weidman TA, Allansmith MR. Branching microvilli in the human conjunctival epithelium. Arch Ophthalmol 1980; 98: 1253–1255

    PubMed  CAS  Google Scholar 

  31. Rohen JW, Lutjen-Drecoll E. Functional morphology of the conjunctiva. IN-The Dry Eye (MA Lemp, R Marquardt R, eds). Springer-Verlag, Berlin. 1992 pp. 35–63

    Google Scholar 

  32. Kenyon KR. The ocular surface. Int Ophthalmol Clin 1979; 1–9(2): 1–35

    Google Scholar 

  33. Gipson IK. Anatomy of the conjunctiva, cornea, and limbus. In: Smolin G, Thoft RA (eds) The cornea. 3rd Edition. Little, Brown & Co., Boston. 1994 pp. 3–24

    Google Scholar 

  34. Nichols BA. Conjunctiva. Microsc Res Techn 1996; 33: 296–321

    Article  CAS  Google Scholar 

  35. Patton DL, Taylor HR. The histopathology of experimental trachoma: ultrastructural changes in the conjunctival epithelium. J Infect Dis 1986; 153: 870–878

    PubMed  CAS  Google Scholar 

  36. Hervouet F, George Y, Tusques J, Ertus M. Aspeet de differentes structures oculaires humaines au microscope a balayage. Bull Soc Franc Ophtalmol 1971; 84: 603–620

    Google Scholar 

  37. Doughty MJ, Panju Z. Exploring the hidden surface of the underside of the eyelid. Contact Lens Spectrum 1995; 19(7): 19–30

    Google Scholar 

  38. Doughty MJ. On the evaluation of the corneal epithelial surface by scanning electron microscopy. Optom Vis Sci 1990; 67: 735–756

    Article  PubMed  CAS  Google Scholar 

  39. Doughty MJ. Analyses of the areas and shapes of cells on the corneal surface of the albino rabbit by scanning electron microscopy. Curr Eye Res 1990; 9: 295–306

    PubMed  CAS  Google Scholar 

  40. Doughty MJ. Scanning electron microscopy study of cell dimensions of rabbit corneal epithelium surface. Cornea 1991; 10: 149–155

    Article  PubMed  CAS  Google Scholar 

  41. Doughty MJ. Evidence for heterogeneity in a small squamous cell type (‘light’ cells) in the rabbit corneal epithelium—a scanning electron microscope study. Doc Ophthalmol 1996; 92: 117–136

    Article  PubMed  Google Scholar 

  42. Clarke SJ, Doughty MJ, Cullen AP. Acute effects of ultraviolet-B irradiation on the corneal surface of the pigmented rabbit studied by quantitative scanning electron microscopy. Acta Ophthalmol 1990; 68: 639–650

    Article  CAS  Google Scholar 

  43. Doughty MJ, Fong WK. Topographical differences in cell area at the surface of corneal epithelium of the pigmented rabbit. Curr Eye Res 1992; 11: 1129–1136

    PubMed  CAS  Google Scholar 

  44. Doughty MJ. A morphometric analysis of the surface cells of rabbit corneal epithelium by scanning electron microscopy. Am J Anat 1990; 189: 316–328

    Article  PubMed  CAS  Google Scholar 

  45. Doughty MJ. Correcting cell density measurements for tissue hydration changes in scanning electron microscopy—application to rabbit corneal endothelium. Tissue Cell 1995; 27: 207–220

    Article  PubMed  CAS  Google Scholar 

  46. Doughty MJ, Stuart DD. Quantification of the hemolysis associated with the use of T-61R euthanasia agent in rabbits—a comparison with pentobarbital sodium and its impact on serum enzyme measurements. Can J Physiol Pharmacol 1995; 73: 1274–1280

    PubMed  CAS  Google Scholar 

  47. Nichols BA, Chiappino ML, Dawson CR. Demonstration of the mucus layer of the tear film by electron microscopy. Invest Ophthalmol Vis Sci 1985; 26: 464–473

    PubMed  CAS  Google Scholar 

  48. Doughty MJ. Evaluation of the effects of saline versus bicarbonate-containing mixed salts solutions on rabbit corneal epitheliumin vitro. Ophthal Physiol Opt 1995; 15: 585–599

    Article  CAS  Google Scholar 

  49. Goller Th and Weyrauch KD. Das Konjunctivalepithel des Hundes. Licht- und elektronenmikroskopische Untersuchungen. Ann Anat 1993; 175: 127–134

    PubMed  CAS  Google Scholar 

  50. Liotet S, Clergue G. Rasterelekronenmikroscopie des Auges. 1985; pp. 14–15

  51. Kessing SV. The mucous gland system of the conjunctiva. Acta Ophthalmol 1968; 95 (suppl): 1–91

    Google Scholar 

  52. Doughty MJ. Acute effects of chlorobutanol- or benzalkonium chloride-containing artificial tears on the surface features of rabbit corneal epithelial cells. Optom Vis Sci 1994; 71: 562–572

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Vision Science, Glasgow-Caledonian University, Cowcaddens Road, G4 0BA, Glasgow, Scotland

    Michael J. Doughty

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  1. Michael J. Doughty
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Correspondence to Michael J. Doughty.

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Doughty, M.J. Scanning electron microscopy study of the tarsal and orbital conjunctival surfaces compared to peripheral corneal epithelium in pigmented rabbits. Doc Ophthalmol 93, 345–371 (1997). https://doi.org/10.1007/BF02569072

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