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A histopathological investigation of Tenon’s capsule in diabetic eyes

International Ophthalmology volume 37, pages 627–633 (2017)Cite this article

Abstract

The aim of this study is to investigate the histopathological features of Tenon’s capsule in eyes with diabetic macular oedema and to compare them between diabetic eyes and healthy subjects. The study included 26 eyes with diabetic oedema and 17 healthy eyes as healthy controls. Tenon’s capsule biopsy specimens were processed with the routine electron microscopic analysis technique. Type I and III collagen fibres were labelled immunohistochemically to determine the amounts of predominating collagen fibres. Leica Q-Win program was used to calculate the amounts of collagen fibres type I and type III and independent-t test was utilized to compare the obtained results between the groups. Statistical significance was set at p < 0.05. Demographic characteristics of both groups were similar (p > 0.05). Collagen type I and type III immunoreactivity was observed both in the control and the diabetic groups. The Amounts of collagen fibres type I and type III were significantly higher in the diabetic group than in the control group (mean collagen type I area: 13.410 ± 0.99 and mean collagen type III area: 23.692 ± 0.17 in the control group; mean collagen type I area: 25.270 ± 6.48 and mean collagen type III area: 28.192 ± 0.82 in the diabetic group. p = 0.0037 for type I and p = 0.0000 for type III). In light of the findings of this study, it can be assumed that diabetes mellitus may engender increased amounts of collagen in Tenon’s capsule. This alteration affecting the success of filtration surgery should be kept in mind especially in diabetic eyes with glaucoma.

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References

  1. Goh SY, Cooper ME (2008) Clinical review: the role of advanced glycation end products in progression and complications of diabetes. J Clin Endocrinol Metab 93:1143–1152

    CAS  Article  PubMed  Google Scholar 

  2. Cooper ME (2004) Importance of advanced glycation end products in diabetes-associated cardiovascular and renal disease. Am J Hypertens 17:31–38

    Article  Google Scholar 

  3. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820

    CAS  Article  PubMed  Google Scholar 

  4. Sheetz MJ, King GL (2002) Molecular understanding of hyperglycemia’s adverse effects for diabetic complications. JAMA 288:2579–2588

    CAS  Article  PubMed  Google Scholar 

  5. Sternberg M, Cohen-Forterre L, Peyroux J (1985) Connective tissue in diabetes mellitus: biochemical alterations of the intercellular matrix with special reference to proteoglycans, collagens and basement membranes. Diabete Metab 11:27–50

    CAS  PubMed  Google Scholar 

  6. Bohlender JM, Franke S, Stein G, Wolf G (2005) Advanced glycation end products and the kidney. Am J Physiol Renal Physiol 289:645–659

    Article  Google Scholar 

  7. Hanna W, Friesen D, Bombardier C, Gladman D, Hanna A (1987) Pathologic features of diabetic thick skin. J Am Acad Dermatol 16:546–553

    CAS  Article  PubMed  Google Scholar 

  8. Bradley JL, King RH, Muddle JR, Thomas PK (2000) The extracellular matrix of peripheral nerve in diabetic polyneuropathy. Acta Neuropathol 99:539–546

    CAS  Article  PubMed  Google Scholar 

  9. Monnier VM, Kohn RR, Cerami A (1984) Accelerated age-related browning of human collagen in diabetes mellitus. Proc Natl Acad Sci USA 81:583–587

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Morello CM (2007) Etiology and natural history of diabetic retinopathy: an overview. Am J Health Syst Pharm 64:3–7

    Article  Google Scholar 

  11. Cheung N, Wong TY (2008) Diabetic retinopathy and systemic vascular complications. Prog Retin Eye Res 27:161–176

    CAS  Article  PubMed  Google Scholar 

  12. Shauly Y, Miller B, Lichtig C, Modan M, Meyer E (1992) Tenon’s capsule: ultrastructure of collagen fibrils in normals and infantile esotropia. Invest Ophthalmol Vis Sci 33:651–656

    CAS  PubMed  Google Scholar 

  13. Meyer E, Ludatscher RM, Miller B, Lichtig C (1992) Connective tissue of the orbital cavity in retinal detachment: an ultrastructural study. Ophthalmic Res 24:365–371

    CAS  Article  PubMed  Google Scholar 

  14. Edelhauser EF, Van Horn DL, Records RE (1990) Cornea and sclera. In: Tasman W, Jaeger EA (eds) Biomedical foundations of ophthalmology, vol vol. 2. J. B. Lippincott, Philadelphia, p 13

    Google Scholar 

  15. Knorr M, Denk PO (1999) Wound healing after glaucoma filtering surgery–a review. Klin Monbl Augenheilkd 214:147–155

    CAS  Article  PubMed  Google Scholar 

  16. Atreides SP, Skuta GL, Reynolds AC (2004) Wound healing modulation in glaucoma filtering surgery. Int Ophthalmol Clin 44:61–106

    Article  PubMed  Google Scholar 

  17. Hugkulstone CE, Smith LF, Vernon SA (1993) Trabeculectomy in diabetic patients with glaucoma. Eye 7:502–506

    Article  PubMed  Google Scholar 

  18. Wong VH, Bui BV, Vingrys AJ (2011) Clinical and experimental links between diabetes and glaucoma. Clin Exp Optom 94:4–23

    Article  PubMed  Google Scholar 

  19. Costa L, Cunha JP, Amado D, Pinto LA, Ferreira J (2015) Diabetes mellitus as a risk factor in glaucoma’s physiopathology and surgical survival time: a literature review. J Curr Glaucoma Pract 9:81–85

    Article  PubMed  Google Scholar 

  20. Browning AC, Alibhai A, McIntosh RS, Rotchford AP, Bhan A, Amoaku WM (2005) Effect of diabetes mellitus and hyperglycemia on the proliferation of human Tenon’s capsule fibroblasts: implications for wound healing after glaucoma drainage surgery. Wound Repair Regen 13:295–302

    Article  PubMed  Google Scholar 

  21. AGIS Investigators. The Advanced Glaucoma Intervention Study (AGIS) (2002) 11. Risk factors for failure of trabeculectomy and argon laser trabeculoplasty. Am J Ophthalmol 134:481–498

    Article  Google Scholar 

  22. Edmunds B, Bunce CV, Thompson JR, Salmon JF, Wormald RP (2004) Factors associated with success in first-time trabeculectomy for patients at low risk of failure with chronic open-angle glaucoma. Ophthalmology 111:97–103

    Article  PubMed  Google Scholar 

  23. Law SK, Hosseini H, Saidi E, Nassiri N, Neelakanta G, Giaconi JA, Caprioli J (2013) Long-term outcomes of primary trabeculectomy in diabetic patients with primary open angle glaucoma. Br J Ophthalmol 97:561–566

    Article  PubMed  Google Scholar 

  24. Haustein UF (1999) Scleroderma-like lesions in insulin-dependent diabetes mellitus. J Eur Acad Dermatol Venereol 13:50–53

    CAS  Article  PubMed  Google Scholar 

  25. Yosipovitch G, Loh KC, Hock OB (2003) Medical pearl: scleroderma-like skin changes in patients with diabetes mellitus. J Am Acad Dermatol 49:109–111

    Article  PubMed  Google Scholar 

  26. Candido R, Forbes JM, Thomas MC et al (2003) A breaker of advanced glycation end products attenuates diabetes-induced myocardial structural changes. Circ Res 92:785–792

    CAS  Article  PubMed  Google Scholar 

  27. Khaw PT, Ward S, Porter A, Grierson I, Hitchings RA, Rice NS (1992) The long-term effects of 5-fluorouracil and sodium butyrate on human Tenon’s fibroblasts. Invest Ophthalmol Vis Sci 33:2043–2052

    CAS  PubMed  Google Scholar 

  28. Saika S, Ooshima A, Yamanaka O et al (1997) In vitro effects of doxorubicin and mitomycin C on human Tenon’s capsule fibroblasts. Ophthalmic Res 29:91–102

    CAS  Article  PubMed  Google Scholar 

  29. Crowston JG, Akbar AN, Constable PH, Occleston NL, Daniels JT, Khaw PT (1998) Antimetabolite-induced apoptosis in Tenon’s capsule fibroblasts. Invest Ophthalmol Vis Sci 39:449–454

    CAS  PubMed  Google Scholar 

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Affiliations

  1. Ankara Ulucanlar Eye Research Hospital, Ulucanlar cad. No: 59 Altındağ, 06100, Ankara, Turkey

    Yasemin Ozdamar Erol & Golge Acaroglu

  2. Department of Histology and Embryology, Hacettepe University Faculty of Medicine, Ankara, Turkey

    Pergin Atilla & Sevda Muftuoglu

  3. Department of Biostatistics, Hacettepe University Faculty of Medicine, Ankara, Turkey

    Jale Karakaya

Authors
  1. Yasemin Ozdamar Erol
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  2. Pergin Atilla
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  3. Golge Acaroglu
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  4. Sevda Muftuoglu
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  5. Jale Karakaya
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Correspondence to Yasemin Ozdamar Erol.

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The authors have no proprietary or financial interest in any of the products used in this study. The authors have no conflict of interest statement.

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Erol, Y.O., Atilla, P., Acaroglu, G. et al. A histopathological investigation of Tenon’s capsule in diabetic eyes. Int Ophthalmol 37, 627–633 (2017). https://doi.org/10.1007/s10792-016-0316-2

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  • DOI: https://doi.org/10.1007/s10792-016-0316-2

Keywords

  • Collagen
  • Connective tissue
  • Diabetes
  • Tenon’s capsule