Collagen Structure and Mechanical Properties of the Human Sclera: Analysis for the Effects of Age

Journal of Biomechanical Engineering

Volumn 137, Issue 4, 2015, Pages

  Coudrillier, Baptiste ^a   Pijanka, Jacek ^b   Jefferys, Joan ^c   Sorensen, Thomas ^d   Quigley, Harry A ^c   Boote, Craig ^b   Nguyen, Thao D ^e  

^a Emory University   (United States)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d DIAMOND LIGHT SOURCE LTD   (United Kingdom)

^e Johns Hopkins University   (United States)

Author keywords

collagen fiber; digital image correlation; finite element model; glaucoma; inverse finite element analysis; sclera; wide angle X ray scattering

Indexed keywords

COLLAGEN; FIBERS; IMAGE ANALYSIS; INVERSE PROBLEMS; MATRIX ALGEBRA; STIFFNESS MATRIX; STRAIN MEASUREMENT; STRUCTURAL PROPERTIES; X RAY SCATTERING;

COLLAGEN FIBER; DIGITAL IMAGE CORRELATIONS; GLAUCOMA; INVERSE FINITE ELEMENT ANALYSIS; SCLERA;

FINITE ELEMENT METHOD;

ADULT; AGE; AGED; ANISOTROPY; ARTICLE; COLLAGEN FIBER; FEMALE; FINITE ELEMENT ANALYSIS; HUMAN; HUMAN TISSUE; MALE; MIDDLE AGED; RADIATION SCATTERING; RIGIDITY; SCLERA; TISSUE STRUCTURE; VERY ELDERLY; AGING; ALGORITHM; BIOMECHANICS; CHEMISTRY; CYTOLOGY; EXTRACELLULAR MATRIX; MECHANICS; METABOLISM;

COLLAGEN;

AGED; AGED, 80 AND OVER; AGING; ALGORITHMS; ANISOTROPY; BIOMECHANICAL PHENOMENA; COLLAGEN; EXTRACELLULAR MATRIX; FEMALE; FINITE ELEMENT ANALYSIS; HUMANS; MALE; MECHANICAL PROCESSES; MIDDLE AGED; SCLERA;

EID: 84930944603     PISSN: 01480731     EISSN: 15288951     Source Type: Journal    
DOI: 10.1115/1.4029430     Document Type: Article

References (65)

1. Watson, P. G., and Young, R. D., 2004, "Scleral Structure, Organisation and Disease. A Review," Exp. Eye Res., 78(3), pp. 609-623.
2. Keeley, F., Morin, J., and Vesely, S., 1984, "Characterization of Collagen From Normal Human Sclera," Exp. Eye Res., 39(5), pp. 533-542.
3. Komai, Y., and Ushiki, T., 1991, "The Three-Dimensional Organization of Collagen Fibrils in the Human Cornea and Sclera," Invest. Ophthalmol. Visual Sci., 32(8), pp. 2244-2258.
4. Kokott, W., 1934, "Das spaltlinienbild der sklera. (ein beitrag zum funktionellen bau der sklera)," Klin. Monatsbl. Augenheilkd, 92, pp. 177-185.
5. Meek, K., and Fullwood, N. J., 2001, "Corneal and Scleral Collagens-A Microscopist's Perspective," Micron, 32(3), pp. 261-272.
6. Yamamoto, S., Hashizume, H., Hitomi, J., Shigeno, M., Sawaguchi, S., Abe, H., and Ushiki, T., 2000, "The Subfibrillar Arrangement of Corneal and Scleral Collagen Fibrils as Revealed by Scanning Electron and Atomic Force Microscopy," Arch. Histol. Cytol., 63(2), pp. 127-135.
7. Marshall, G., Konstas, A., and Lee, W., 1993, "Collagens in Ocular Tissues," Br. J. Ophthalmol., 77(8), pp. 515-524.
8. Winkler, M., Jester, B., Nien-Shy, C., Massei, S., Minckler, D. S., Jester, J. V., and Brown, D. J., 2010, "High Resolution Three-Dimensional Reconstruction of the Collagenous Matrix of the Human Optic Nerve Head," Brain Res. Bull., 81(2), pp. 339-348.
9. Yan, D., McPheeters, S., Johnson, G., Utzinger, U., and Geest, J. P. V., 2011, "Microstructural Differences in the Human Posterior Sclera as a Function of Age and Race," Invest. Ophthalmol. Visual Sci., 52(2), pp. 821-829.
10. Danford, F. L., Yan, D., Dreier, R. A., Cahir, T. M., Girkin, C. A., and Geest, J. P. V., 2013, "Differences in the Region-and Depth-Dependent Microstructural Organization in Normal Versus Glaucomatous Human Posterior Sclerae," Invest. Ophthalmol. Visual Sci., 54(13), pp. 7922-7932.
11. Girard, M. J., Dahlmann-Noor, A., Rayapureddi, S., Bechara, J. A., Bertin, B. M., Jones, H., Albon, J., Khaw, P. T., and Ethier, C. R., 2011, "Quantitative Mapping of Scleral Fiber Orientation in Normal Rat Eyes," Invest. Ophthalmol. Visual Sci., 52(13), pp. 9684-9693.
12. Pijanka, J. K., Coudrillier, B., Ziegler, K., Sorensen, T., Meek, K. M., Nguyen, T. D., Quigley, H. A., and Boote, C., 2012, "Quantitative Mapping of Collagen Fiber Orientation in Non-Glaucoma and Glaucoma Posterior Human Sclerae," Invest. Ophthalmol. Visual Sci., 53(9), pp. 5258-5270.
13. Pijanka, J. K., Abass, A., Sorensen, T., Elsheikh, A., and Boote, C., 2013, "A Wide-Angle X-Ray Fibre Diffraction Method for Quantifying Collagen Orientation Across Large Tissue Areas: Application to the Human Eyeball Coat," J. Appl. Crystallogr., 46(5), pp. 1481-1489.
14. Coudrillier, B., Boote, C., Quigley, H. A., and Nguyen, T. D., 2013, "Scleral Anisotropy and its Effects on the Mechanical Response of the Optic Nerve Head," Biomech. Model. Mechanobiol., 12(5), pp. 941-963.
15. Rada, J. A., Achen, V. R., Penugonda, S., Schmidt, R. W., and Mount, B. A., 2000, "Proteoglycan Composition in the Human Sclera During Growth and Aging," Invest. Ophthalmol. Visual Sci., 41(7), pp. 1639-1648.
16. Lewis, P. N., Pinali, C., Young, R. D., Meek, K. M., Quantock, A. J., and Knupp, C., 2010, "Structural Interactions Between Collagen and Proteoglycans are Elucidated by Three-Dimensional Electron Tomography of Bovine Cornea," Structure, 18(2), pp. 239-245.
17. Girard, M. J., Suh, J.-K. F., Bottlang, M., Burgoyne, C. F., and Downs, J. C., 2009, "Scleral Biomechanics in the Aging Monkey Eye," Invest. Ophthalmol. Visual Sci., 50(11), pp. 5226-5237.
18. Coudrillier, B., Tian, J., Alexander, S., Myers, K. M., Quigley, H. A., and Nguyen, T. D., 2012, "Biomechanics of the Human Posterior Sclera: Age-and Glaucoma-Related Changes Measured Using Inflation Testing," Invest. Ophthalmol. Visual Sci., 53(4), pp. 1714-1728.
19. Malik, N. S., Moss, S. J., Ahmed, N., Furth, A. J., Wall, R. S., and Meek, K. M., 1992, "Ageing of the Human Corneal Stroma: Structural and Biochemical Changes," Biochim. Biophys. Acta, Mol. Basis Dis., 1138(3), pp. 222-228.
20. Bailey, A. J., Paul, R. G., and Knott, L., 1998, "Mechanisms of Maturation and Ageing of Collagen," Mech. Ageing Dev., 106(1), pp. 1-56.
21. Geraghty, B., Jones, S. W., Rama, P., Akhtar, R., and Elsheikh, A., 2012, "Age-Related Variations in the Biomechanical Properties of Human Sclera," J. Mech. Behav. Biomed. Mater., 16, pp. 181-191.
22. Grytz, R., Fazio, M. A., Libertiaux, V., Bruno, L., Gardiner, S. K., Girkin, C. A., and Downs, J. C., 2014, "Age-and Race-Related Differences in Human Scleral Material Properties," Invest. Ophthalmol. Visual Sci., 55(12), pp. 8163-8172.
23. Myers, K. M., Cone, F. E., Quigley, H. A., Gelman, S., Pease, M. E., and Nguyen, T. D., 2010, "The in Vitro Inflation Response of Mouse Sclera," Exp. Eye Res., 91(6), pp. 866-875.
24. Fazio, M. A., Grytz, R., Morris, J. S., Bruno, L., Gardiner, S. K., Girkin, C. A., and Downs, J. C., 2014, "Age-Related Changes in Human Peripapillary Scleral Strain," Biomech. Model. Mechanobiol., 13(3), pp. 551-563.
25. Fazio, M. A., Grytz, R., Morris, J. S., Bruno, L., Girkin, C. A., and Downs, J. C., 2014, "Human Scleral Structural Stiffness Increases More Rapidly With Age in Donors of African Descent Compared to Donors of European Descent," Invest. Ophthalmol. Visual Sci., 55(11), pp. 7189-7198.
26. Foster, A., and Resnikoff, S., 2005, "The Impact of Vision 2020 on Global Blindness," Eye, 19(10), pp. 1133-1135.
27. Quigley, H., Hohman, R., Addicks, E., Massof, R., and Green, W. R., 1983, "Morphologic Changes in the Lamina Cribrosa Correlated With Neural Loss in Open-Angle Glaucoma," Am. J. Ophthalmol., 95(5), pp. 673-691.
28. Fechtner, R. D., and Weinreb, R. N., 1994, "Mechanisms of Optic Nerve Damage in Primary Open Angle Glaucoma," Surv. Ophthalmol., 39(1), pp. 23-42.
29. Burgoyne, C. F., Crawford Downs, J., Bellezza, A. J., Francis Suh, J.-K., and Hart, R. T., 2005, "The Optic Nerve Head as a Biomechanical Structure: A New Paradigm for Understanding the Role of IOP-Related Stress and Strain in the Pathophysiology of Glaucomatous Optic Nerve Head Damage," Prog. Retinal Eye Res., 24(1), pp. 39-73.
30. Campbell, I. C., Coudrillier, B., and Ethier, C. R., 2014, "Biomechanics of the Posterior Eye: A Critical Role in Health and Disease," ASME J. Biomech. Eng., 136(2), p. 021005.
31. Quigley, H. A., and Vitale, S., 1997, "Models of Open-Angle Glaucoma Prevalence and Incidence in the United States," Invest. Ophthalmol. Visual Sci., 38(1), pp. 83-91.
32. Boland, M. V., and Quigley, H. A., 2007, "Risk Factors and Open-Angle Glaucoma: Classification and Application," J. Glaucoma, 16(4), pp. 406-418.
33. Leske, M. C., Wu, S.-Y., Hennis, A., Honkanen, R., and Nemesure, B., 2008, "Risk Factors for Incident Open-Angle Glaucoma: The Barbados Eye Studies," Ophthalmology, 115(1), pp. 85-93.
34. Broman, A. T., Quigley, H. A., West, S. K., Katz, J., Munoz, B., Bandeen-Roche, K., Tielsch, J. M., Friedman, D. S., Crowston, J., Taylor, H. R., Varma, R., Leske, M. C., Bengtsson, B., Heijl, A., He, M., and Foster, P. J., 2008, "Estimating the Rate of Progressive Visual Field Damage in Those With Open-Angle Glaucoma, From Cross-Sectional Data," Invest. Ophthalmol. Visual Sci., 49(1), pp. 66-76.
35. Sigal, I. A., Flanagan, J. G., and Ethier, C. R., 2005, "Factors Influencing Optic Nerve Head Biomechanics," Invest. Ophthalmol. Visual Sci., 46(11), pp. 4189-4199.
36. Sigal, I. A., Yang, H., Roberts, M. D., Grimm, J. L., Burgoyne, C. F., Demirel, S., and Downs, J. C., 2011, "IOP-Induced Lamina Cribrosa Deformation and Scleral Canal Expansion: Independent or Related?," Invest. Ophthalmol. Visual Sci., 52(12), pp. 9023-9032.
37. Norman, R. E., Flanagan, J. G., Sigal, I. A., Rausch, S. M., Tertinegg, I., and Ethier, C. R., 2011, "Finite Element Modeling of the Human Sclera: Influence on Optic Nerve Head Biomechanics and Connections With Glaucoma," Exp. Eye Res., 93(1), pp. 4-12.
38. Burgoyne, C. F., and Downs, J. C., 2008, "Premise and Prediction-How Optic Nerve Head Biomechanics Underlies the Susceptibility and Clinical Behavior of the Aged Optic Nerve Head," J. Glaucoma, 17(4), pp. 318-328.
39. McBrien, N. A., Jobling, A. I., and Gentle, A., 2009, "Biomechanics of the Sclera in Myopia: Extracellular and Cellular Factors," Optom. Vision Sci., 86(1), pp. E23-E30.
40. Summers Rada, J. A., Shelton, S., and Norton, T. T., 2006, "The Sclera and Myopia," Exp. Eye Res., 82(2), pp. 185-200.
41. Myers, K. M., Coudrillier, B., Boyce, B. L., and Nguyen, T. D., 2010, "The Inflation Response of the Posterior Bovine Sclera," Acta Biomater., 6(11), pp. 4327-4335.
42. Tonge, T., Murienne, B., Coudrillier, B., Alexander, S., Rothkopf, W., and Nguyen, D., 2013, "Minimal Preconditioning Effects Observed for Inflation Tests of Planar Tissues," ASME J. Biomech. Eng., 135(11), p. 114502.
43. Ke, X.-D., Schreier, H., Sutton, M., and Wang, Y., 2011, "Error Assessment in Stereo-Based Deformation Measurements," Exp. Mech., 51(4), pp. 423-441.
44. Fazzini, M., Mistou, S., and Dalverny, O., 2010, "Error Assessment in Image Stereo-Correlation," EPJ Web of Conferences, Vol. 6, EDP Sciences, p. 31009.
45. Boote, C., Dennis, S., Huang, Y., Quantock, A. J., and Meek, K. M., 2005, "Lamellar Orientation in Human Cornea in Relation to Mechanical Properties," J. Struct. Biol., 149(1), pp. 1-6.
46. Boote, C., Hayes, S., Abahussin, M., and Meek, K. M., 2006, "Mapping Collagen Organization in the Human Cornea: Left and Right Eyes Are Structurally Distinct," Invest. Ophthalmol. Visual Sci., 47(3), pp. 901-908.
47. Ren, R., Wang, N., Li, B., Li, L., Gao, F., Xu, X., and Jonas, J. B., 2009, "Lamina Cribrosa and Peripapillary Sclera Histomorphometry in Normal and Advanced Glaucomatous Chinese Eyes With Various Axial Length," Invest. Ophthalmol. Visual Sci., 50(5), pp. 2175-2184.
48. Norman, R. E., Flanagan, J. G., Rausch, S. M., Sigal, I. A., Tertinegg, I., Eilaghi, A., Portnoy, S., Sled, J. G., and Ethier, C. R., 2010, "Dimensions of the Human Sclera: Thickness Measurement and Regional Changes With Axial Length," Exp. Eye Res., 90(2), pp. 277-284.
49. Vurgese, S., Panda-Jonas, S., and Jonas, J. B., 2012, "Scleral Thickness in Human Eyes," PloS One, 7(1), p. e29692.
50. Jonas, J. B., and Holbach, L., 2005, "Central Corneal Thickness and Thickness of the Lamina Cribrosa in Human Eyes," Invest. Ophthalmol. Visual Sci., 46(4), pp. 1275-1279.
51. Girard, M. J., Suh, J.-K. F., Bottlang, M., Burgoyne, C. F., and Downs, J. C., 2011, "Biomechanical Changes in the Sclera of Monkey Eyes Exposed to Chronic IOP Elevations," Invest. Ophthalmol. Visual Sci., 52(8), pp. 5656-5669.
52. Grytz, R., Fazio, M. A., Girard, M. J., Libertiaux, V., Bruno, L., Gardiner, S., Girkin, C. A., and Crawford Downs, J., 2014, "Material Properties of the Posterior Human Sclera," J. Mech. Behav. Biomed. Mater. 29, pp. 602-617.
53. Seshaiyer, P., and Humphrey, J. D., 2003, "A Sub-Domain Inverse Finite Element Characterization of Hyperelastic Membranes Including Soft Tissues," ASME J. Biomech. Eng., 125(3), pp. 363-371.
54. Raghupathy, R., and Barocas, V. H., 2010, "Generalized Anisotropic Inverse Mechanics for Soft Tissues," ASME J. Biomech. Eng., 132(8), p. 081006.
55. Pinsky, P. M., van der Heide, D., and Chernyak, D., 2005, "Computational Modeling of Mechanical Anisotropy in the Cornea and Sclera," J. Cataract Refractive Surg., 31(1), pp. 136-145.
56. Brown, C., Vural, M., Johnson, M., and Trinkaus-Randall, V., 1994, "Age-Related Changes of Scleral Hydration and Sulfated Glycosaminoglycans," Mech. Ageing Dev., 77(2), pp. 97-107.
57. Eilaghi, A., Flanagan, J. G., Tertinegg, I., Simmons, C. A., Wayne Brodland, G., and Ross Ethier, C., 2010, "Biaxial Mechanical Testing of Human Sclera," J. Biomech., 43(9), pp. 1696-1701.
58. Chen, K., Rowley, A. P., Weiland, J. D., and Humayun, M. S., 2013, "Elastic Properties of Human Posterior Eye," J. Biomed. Mater. Res. Part A, 102(6), pp. 2001-2007.
59. Hernandez, M. R., Luo, X. X., Igoe, F., and Neufeld, A., 1987, "Extracellular Matrix of the Human Lamina Cribrosa," Am. J. Ophthalmol., 104(6), pp. 567-576.
60. Quigley, H. A., Brown, A., and Dorman-Pease, M. E., 1991, "Alterations in Elastin of the Optic Nerve Head in Human and Experimental Glaucoma," Br. J. Ophthalmol., 75(9), pp. 552-557.
61. Meek, K. M., and Boote, C., 2009, "The Use of X-Ray Scattering Techniques to Quantify the Orientation and Distribution of Collagen in the Corneal Stroma," Prog. Retinal Eye Res., 28(5), pp. 369-392.
62. Petsche, S. J., and Pinsky, P. M., 2013, "The Role of 3-D Collagen Organization in Stromal Elasticity: A Model Based on X-Ray Diffraction Data and Second Harmonic-Generated Images," Biomech. Model. Mechanobiol., 12(6), pp. 1101-1113.
63. Fazio, M. A., Grytz, R., Bruno, L., Girard, M. J., Gardiner, S., Girkin, C. A., and Downs, J. C., 2012, "Regional Variations in Mechanical Strain in the Posterior Human Sclera," Invest. Ophthalmol. Visual Sci., 53(9), pp. 5326-5333.
64. Tang, J., and Liu, J., 2012, "Ultrasonic Measurement of Scleral Cross-Sectional Strains During Elevations of Intraocular Pressure: Method Validation and Initial Results in Posterior Porcine Sclera," ASME J. Biomech. Eng., 134(9), p. 091007.
65. Morris, H. J., Tang, J., Cruz-Perez, B., Pan, X., Hart, R. T., Weber, P. A., and Liu, J., 2013, "Correlation Between Biomechanical Responses of Posterior Sclera and Iop Elevations During Micro-Volumetric Change in the Eye," Invest. Ophthalmol. Visual Sci., 54(12), pp. 7215-7222.