Shear behavior of bovine scleral tissue

Journal of Biomechanical Engineering

Volumn 136, Issue 7, 2014, Pages

  Argento, Alan ^a   Kim, Wonsuk ^a   Rozsa, Frank W ^b   DeBolt, Kori L ^a   Zikanova, Sophia ^a   Richards, Julia R ^a  

^a Department of Electrical and Computer Engineering   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EYE PROTECTION; MAMMALS; SHEAR FLOW; TISSUE;

ANATOMICAL STUDIES; CONTROLLED TEMPERATURE; MECHANICAL BEHAVIOR; OUT-OF-PLANE MODES; PRIMARY OPEN ANGLE GLAUCOMAS; SPECIMEN ORIENTATION; TENSION AND COMPRESSION; VISCOSITY COEFFICIENT;

TISSUE ENGINEERING;

ANIMAL TISSUE; ARTICLE; BEEF CATTLE; FORCE TRANSDUCER; HUMIDITY; HYDRATION; NONHUMAN; OPTIC NERVE; PHYSICAL PHENOMENA; RELAXATION TIME; SCLERA; SHEAR BEHAVIOR; SHEAR STRESS; STRESS STRAIN RELATIONSHIP; SURFACE PROPERTY; TEMPERATURE; VELOCITY; VISCOELASTICITY; VISCOSITY; VITREOUS BODY; WEIGHT BEARING; ANIMAL; BIOMECHANICS; BOVINE; CYTOLOGY; INNERVATION; MATERIALS TESTING; MECHANICAL STRESS; SHEAR STRENGTH;

ANIMALS; BIOMECHANICAL PHENOMENA; CATTLE; MATERIALS TESTING; OPTIC NERVE; SCLERA; SHEAR STRENGTH; STRESS, MECHANICAL; TEMPERATURE;

EID: 84901478554     PISSN: 01480731     EISSN: 15288951     Source Type: Journal    
DOI: 10.1115/1.4027615     Document Type: Article

References (84)

1. Burgoyne, C. F., 2010, Optic Nerve: The Glaucomatous Optic Nerve, Springer Berlin, Heidelberg.
2. Strouthidis, N. G., and Girard, M. J. A., 2013, "Altering the Way the Optic Nerve Head Responds to Intraocular Pressure-A Potential Approach to Glaucoma Therapy," Curr. Opin. Pharmacol., 13(1), pp. 83-89.
3. Shah, S., Laiquzzaman, M., Bhojwani, R., Mantry, S., and Cunliffe, I., 2007, "Assessment of the Biomechanical Properties of the Cornea With the Ocular Response Analyzer in Normal and Keratoconic Eyes," Invest. Ophthalmol. Visual Sci., 48(7), pp. 3026-3031. (Pubitemid 351261143)
4. Gefen, A., Shalom, R., Elad, D., and Mandel, Y., 2009, "Biomechanical Analysis of the Keratoconic Cornea," J. Mech. Behav. Biomed. Mater., 2(3), pp. 224-236.
5. Dupps, J. W. J., 2007, "Hysteresis: New Mechanospeak for the Ophthalmologist," J. Cataract Refractive Surg., 33(9), pp. 1499-1501.
6. Fraldi, M., Cutolo, A., Esposito, L., and Guarracino, F., 2011, "The Role of Viscoelasticity and Stress Gradients on the Outcome of Conductive Keratoplasty," Biomech. Model. Mechanobiol., 10(3), pp. 397-412.
7. Shah, S., Laiquzzaman, M., Cunliffe, I., and Mantry, S., 2006, "The Use of the Reichert Ocular Response Analyser to Establish the Relationship Between Ocular Hysteresis, Corneal Resistance Factor and Central Corneal Thickness in Normal Eyes," Contact Lens Anterior Eye, 29(5), pp. 257-262. (Pubitemid 44743122)
8. Ethier, C. R., Johnson, M., and Ruberti, J., 2004, "Ocular Biomechanics and Biotransport," Ann. Rev. Biomed. Eng., 6(1), pp. 249-273. (Pubitemid 39209499)
9. Kennedy, E., and Duma, S., 2008, "The Effects of the Extraocular Muscles on Eye Impact Force-Deflection and Globe Rupture Response," J. Biomech., 41(16), pp. 3297-3302.
10. Kenney, K. S., and Fanciullo, L. M., 2005, "Automobile Air Bags: Friend or Foe A Case of Air Bag-Associated Ocular Trauma and a Related Literature Review," Optom.-J. Am. Optom. Assoc., 76(7), pp. 382-386. (Pubitemid 41296787)
11. Rangarajan, N., Kamalakkannan, S. B., Hasija, V., Shams, T., Jenny, C., Serbanescu, I., Ho, J., Rusinek, M., and Levin, A. V., 2009, "Finite Element Model of Ocular Injury in Abusive Head Trauma," J. Am. Assoc. Pediatr. Ophthalmol. Strabismus, 13(4), pp. 364-369.
12. Stitzel, J. D., Duma, S. M., Cormier, J. M., and Herring, I. P., 2002, "A Nonlinear Finite Element Model of the Eye With Experimental Validation for the Prediction of the Globe Rupture," Stapp Car Crash J., 46, pp. 81-102.
13. Stitzel, J. D., Hansen, G. A., Herring, I. P., and Duma, S. M., 2005, "Blunt Trauma of the Aging Eye-Injury Mechanisms and Increasing Lens Stiffness," Arch. Ophthalmol., 123(6), pp. 789-794. (Pubitemid 41056600)
14. Uchio, E., Ohno, S., Kudoh, K., Kadonosono, K., Andoh, K., and Kisielewicz, L. T., 2001, "Simulation of Air-Bag Impact on Post-Radial Keratotomy Eye Using Finite Element Analysis," J. Cataract Refractive Surg., 27(11), pp. 1847-1853. (Pubitemid 33055557)
15. Johnson, C. S., Mian, S. I., Moroi, S., Epstein, D., Izatt, J., and Afshari, N. A., 2007, "Role of Corneal Elasticity in Damping of Intraocular Pressure," Invest. Ophthalmol. Visual Sci., 48(6), pp. 2540-2544. (Pubitemid 351261203)
16. Siegwart, J. J. T., and Norton, T. T., 1999, "Regulation of the Mechanical Properties of Tree Shrew Sclera by the Visual Environment," Vision Res., 39(2), pp. 387-407. (Pubitemid 29052382)
17. Hoeltzel, D. A., Altman, P., Buzard, K., and Choe, K. I., 1992, "Strip Extensiometry for Comparison of the Mechanical Response of Bovine, Rabbit, and Human Corneas," ASME J. Biomech. Eng., 114(2), pp. 202-215.
18. Friberg, T. R., and Lace, J. W., 1988, "A Comparison of the Elastic Properties of Human Choroid and Sclera," Exp. Eye Res., 47(3), pp. 429-436.
19. Asejczyk-Widlicka, M., and Pierscionek, B. K., 2008, "The Elasticity and Rigidity of the Outer Coats of the Eye," Br. J. Ophthalmol., 92(10), pp. 1415-1418.
20. Asejczyk-Widlicka, M., -Sr-odka, W., Schachar, R. A., and Pier-scionek, B. K., 2011, "Material Properties of the Cornea and Sclera: A Modelling Approach to Test Experimental Analysis," J. Biomech., 44(3), pp. 543-546.
21. Downs, J. C., Suh, J. K. F., Thomas, K. A., Bellezza, A. J., Burgoyne, C. F., and Hart, R. T., 2003, "Viscoelastic Characterization of Peripapillary Sclera: Material Properties by Quadrant in Rabbit and Monkey Eyes," ASME J. Biomech. Eng., 125(1), pp. 124-131. (Pubitemid 36297235)
22. Kim, W., Argento, A., Rozsa, F. W., and Mallett, K., 2012, "Constitutive Behavior of Ocular Tissues Over a Range of Strain Rates," ASME J. Biomech. Eng., 134(6), p. 061002.
23. Downs, J. C., Suh, J. K. F., Thomas, K. A., Bellezza, A. J., Hart, R. T., and Burgoyne, C. F., 2005, "Viscoelastic Material Properties of the Peripapillary Sclera in Normal and Early-Glaucoma Monkey Eyes," Invest. Ophthalmol. Visual Sci., 46(2), pp. 540-546. (Pubitemid 40270333)
24. Nguyen, T. D., Jones, R. E., and Boyce, B. L., 2008, "A Nonlinear Anisotropic Viscoelastic Model for the Tensile Behavior of the Corneal Stroma," ASME J. Biomech. Eng., 130(4), p. 041020.
25. Boyce, B. L., Jones, R. E., Nguyen, T. D., and Grazier, J. M., 2007, "Stress-Controlled Viscoelastic Tensile Response of Bovine Cornea," J. Biomech., 40(11), pp. 2367-2376. (Pubitemid 47081028)
26. Bisplinghoff, J. A., Mcnally, C., Brozoski, F. T., and Duma, S. M., 2008, "Dynamic Material Property Measurements of Human Eyes," Biomed. Sci. Instrum., 44, pp. 177-182. (Pubitemid 351619685)
27. 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.
28. Mattson, M. S., Huynh, J.,Wiseman,M., Coassin, M., Kornfield, J. A., and Schwartz, D. M., 2010, "An in vitro Intact Globe Expansion Method for Evaluation of Cross-Linking Treatments," Invest. Ophthalmol. Visual Sci., 51(6), pp. 3120-3128.
29. Thornton, I. L., Dupps, W. J., Roy, A. S., and Krueger, R. R., 2009, "Biomechanical Effects of Intraocular Pressure Elevation on Optic Nerve/Lamina Cribrosa Before and After Peripapillary Scleral Collagen Cross-Linking," Invest. Ophthalmol. Visual Sci., 50(3), pp. 1227-1233.
30. Liu, J., and He, X., 2009, "Corneal Stiffness Affects IOP Elevation During Rapid Volume Change in the Eye," Invest. Ophthalmol. Visual Sci., 50(5), pp. 2224-2229.
31. Litwiller, D., Lee, S., Kolipaka, A., Mariappan, Y., Glaser, K., Pulido, J., and Ehman, R., 2010, "MR Elastography of the Ex Vivo Bovine Globe," J. Mag. Reson. Imaging, 32(1), pp. 44-51.
32. Coudrillier, B., Boote, C., Quigley, H., and Nguyen, T., 2013, "Scleral Anisotropy and Its Effects on the Mechanical Response of the Optic Nerve Head," Biomech. Model. Mechanobiol., 12(5), pp. 941-963.
33. 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," Investig. Ophthalmol. Visual Sci., 53(4), pp. 1714-1728.
34. Fazio, M., Grytz, R., Morris, J., Bruno, L., Gardiner, S., Girkin, C., and Downs, J. C., 2014, "Age-Related Changes in Human Peripapillary Scleral Strain," Biomech. Model. Mechanobiol., 13(3), pp. 551-563.
35. Girard, M. J. A., Downs, J. C., Bottlang, M., Burgoyne, C. F., and Suh, J. K. F., 2009, "Peripapillary and Posterior Scleral Mechanics-Part II: Experimental and Inverse Finite Element Characterization," ASME J. Biomech. Eng., 131(5), p. 051012.
36. 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.
37. Woo, S. L. Y., Schlegel, W. A., Kobayash., A. S., and Lawrence, C., 1972, "Nonlinear Material Properties of Intact Cornea and Sclera," Exp. Eye Res., 14(1), pp. 29-39.
38. Grytz, R., Fazio, M. A., Girard, M. J. A., 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.
39. Nguyen, T. D., and Boyce, B. L., 2011, "An Inverse Finite Element Method for Determining the Anisotropic Properties of the Cornea," Biomech. Model. Mechanobiol., 10(3), pp. 323-337.
40. Spoerl, E., Boehm, A. G., and Pillunat, L. E., 2005, "The Influence of Various Substances on the Biomechanical Behavior of Lamina Cribrosa and Peripapillary Sclera," Invest. Ophthalmol. Visual Sci., 46(4), pp. 1286-1290. (Pubitemid 41685866)
41. Albon, J., Purslow, P. P., Karwatowski, W. S., and Easty, D. L., 2000, "Age Related Compliance of the Lamina Cribrosa in Human Eyes," Br. J. Ophthalmol., 84(3), pp. 318-323. (Pubitemid 30251690)
42. 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. (Pubitemid 39535155)
43. Eilaghi, A., Flanagan, J. G., Tertinegg, I., Simmons, C. A., Brodland, G. W., and Ethier, C. R., 2010, "Biaxial Mechanical Testing of Human Sclera," J. Biomech., 43, pp. 1696-1701.
44. Eilaghi, A., Flanagan, J. G., Simmons, C. A., and Ethier, C. R., 2010, "Effects of Scleral Stiffness Properties on Optic Nerve Head Biomechanics," Ann. Biomed. Eng., 38(4), pp. 1586-1592.
45. Grytz, R., Girkin, C. A., Libertiaux, V., and Downs, J. C., 2012, "Perspectives on Biomechanical Growth and Remodeling Mechanisms in Glaucoma," Mech. Res. Commun., 42, pp. 92-106.
46. Grytz, R., Meschke, G., and Jonas, J. B., 2011, "The Collagen Fibril Architecture in the Lamina Cribrosa and Peripapillary Sclera Predicted by a Computational Remodeling Approach," Biomech. Model. Mechanobiol., 10(3), pp. 371-382.
47. Quigley, H. A., Dorman-Pease, M. E., and Brown, A. E., 1991, "Quantitative Study of Collagen and Elastin of the Optic Nerve Head and Sclera in Human and Experimental Monkey Glaucoma," Curr. Eye Res., 10(9), pp. 877-888.
48. Girard, M. J. A., Dahlmann-Noor, A., Rayapureddi, S., Bechara, J. A., Bertin, B. M. E., 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.
49. Girard, M. J. A., Downs, J. C., Burgoyne, C. F., and Suh, J. K. F., 2009, "Peripapillary and Posterior Scleral Mechanics-Part I: Development of an Anisotropic Hyperelastic Constitutive Model," ASME J. Biomech. Eng., 131(5), p. 051011.
50. Danford, F. L., Yan, D., Dreier, R. A., Cahir, T. M., Girkin, C. A., and Vande Geest, J. P., 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.
51. Triyoso, D. H., and Good, T. A., 1999, "Pulsatile Shear Stress Leads to DNA Fragmentation in Human SH-SY5Y Neuroblastoma Cell Line," J. Physiol., 515(2), pp. 355-365. (Pubitemid 29129207)
52. Battaglioli, J. L., and Kamm, R. D., 1984, "Measurements of the Compressive Properties of Scleral Tissue," Invest. Ophthalmol. Visual Sci., 25(1), pp. 59-65. (Pubitemid 14220988)
53. Mortazavi, A. M., Simon, B. R., Stamer, W. D., and Vande Geest, J. P., 2009, "Drained Secant Modulus for Human and Porcine Peripapillary Sclera Using Unconfined Compression Testing," Exp. Eye Res., 89(6), pp. 892-897.
54. Gardiner, J. C., and Weiss, J. A., 2001, "Simple Shear Testing of Parallel-Fibered Planar Soft Tissues," ASME J. Biomech. Eng., 123(2), pp. 170-175. (Pubitemid 32385201)
55. Talman, E. A., and Boughner, D. R., 2001, "Effect of Altered Hydration on the Internal Shear Properties of Porcine Aortic Valve Cusps," Ann. Thorac. Surg., 71(5 Suppl), pp. S375-S378. (Pubitemid 32437001)
56. Magnussen, R. A., Guilak, F., and Vail, T. P., 2005, "Cartilage Degeneration in Post-Collapse Cases of Osteonecrosis of the Human Femoral Head: Altered Mechanical Properties in Tension, Compression, and Shear," J. Orthop. Res., 23(3), pp. 576-583. (Pubitemid 40631329)
57. Bonifasi-Lista, C., Lake, S. P., Small, M. S., and Weiss, J. A., 2005, "Viscoelastic Properties of the Human Medial Collateral Ligament under Longitudinal, Transverse and Shear Loading," J. Orthop. Res., 23(1), pp. 67-76. (Pubitemid 40045079)
58. Sacks, M. S., 1999, "A Method for Planar Biaxial Mechanical Testing That Includes In-Plane Shear," ASME J. Biomech. Eng., 121(5), pp. 551-555. (Pubitemid 29503186)
59. Cruz-Perez, B., Tang, J., Morris, H. J., Palko, J. R., Pan, X., Hart, R. T., and Liu, J., 2014, "Biaxial Mechanical Testing of Posterior Sclera Using High-Resolution Ultrasound Speckle Tracking for Strain Measurements," J. Biomech., 47(5), pp. 1151-1156.
60. Schmut, O., 1977, "The Identification of Type III Collagen in Calf and Bovine Cornea and Sclera," Exp. Eye Res., 25(5), pp. 505-509. (Pubitemid 8237827)
61. Siddiqi, N. J., Sharma, B., and Alhomida, A. S., 2001, "A Study on Distribution of Different Hydroxyproline Fractions in the Bovine Ocular Tissues," Mol. Cell. Biochem., 217(1-2), pp. 67-71. (Pubitemid 32184457)
62. Trier, K., 2005, "The Sclera," Advances in Organ Biology, 10, Elsevier B.V., pp. 353-373. (Pubitemid 43588821)
63. 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. (Pubitemid 30459128)
64. Maurice, D. M., and Polgar, J., 1977, "Diffusion Across the Sclera," Exp. Eye Res., 25(6), pp. 577-582. (Pubitemid 8246490)
65. Olsen, T. W., Edelhauser, H. F., Lim, J. I., and Geroski, D. H., 1995, "Human Scleral Permeability. Effects of Age, Cryotherapy, Transscleral Diode Laser, and Surgical Thinning," Invest. Ophthalmol. Visual Sci., 36(9), pp. 1893-1903.
66. Budras, K. D., Habel, R. E., Mulling, C. K. W., and Greenough, P. R., 2011, Bovine Anatomy: An Illustrated Text, Manson Publishing, Hannover, Germany.
67. Fung, Y. C., 1965, Foundations of Solid Mechanics, Prentice-Hall International Series in Dynamics, Prentice-Hall, Englewood Cliffs, N.J.
68. Negahban, M., 2012, The Mechanical and Thermodynamical Theory of Plasticity, CRC Press, Boca Raton, FL.
69. Bartel, D. L., Davy, D. T., and Keaveny, T. M., 2006, Orthopaedic Biomechanics: Mechanics and Design in Musculoskeletal Systems, Pearson/Prentice Hall, Upper Saddle River, NJ.
70. Mitra, S., Ghanbari-Siahkali, A., and Almdal, K., 2006, "A Novel Method for Monitoring Chemical Degradation of Crosslinked Rubber by Stress Relaxation Under Tension," Polym. Degrad. Stab., 91(10), pp. 2520-2526. (Pubitemid 43977784)
71. Welch, B. L., 1951, "On the Comparison of Several Mean Values: An Alternative Approach," Biometrika, 38(3/4), pp. 330-336.
72. Zeng, Y., Yang, J., Huang, K., Lee, Z., and Lee, X., 2001, "A Comparison of Biomechanical Properties Between Human and Porcine Cornea," J. Biomech., 34(4), pp. 533-537. (Pubitemid 32215480)
73. 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.
74. Moses, R. A., Grodzki, J. W. J., Starcher, B. C., and Galione, M. J., 1978, "Elastin Content of the Scleral Spur, Trabecular Mesh, and Sclera," Invest. Ophthalmol. Visual Sci., 17(8), pp. 817-818. (Pubitemid 8382971)
75. Rada, J. A., Achen, V. R., Perry, C. A., and Fox, P. W., 1997, "Proteoglycans in the Human Sclera. Evidence for the Presence of Aggrecan," Invest. Ophthalmol. Visual Sci., 38(9), pp. 1740-1751. (Pubitemid 27382339)
76. Cheng, T., and Gan, R. Z., 2008, "Experimental Measurement and Modeling Analysis on Mechanical Properties of Tensor Tympani Tendon," Med. Eng. Phys., 30(3), pp. 358-366. (Pubitemid 351318287)
77. Girard, M., Suh, J.-K. F., Hart, R. T., Burgoyne, C. F., and Downs, J. C., 2007, "Effects of Storage Time on the Mechanical Properties of Rabbit Peripapillary Sclera after Enucleation," Curr. Eye Res., 32(5), pp. 465-470. (Pubitemid 46789428)
78. Gum, G. G., Gelatt, K. N., Miller, D. N., and Mackay, E. O., 1998, "Intraocular Pressure in Normal Dairy Cattle," Vet. Ophthalmol., 1(2-3), pp. 159-161. (Pubitemid 128490974)
79. Cheng, S., Clarke, E. C., and Bilston, L. E., 2009, "The Effects of Preconditioning Strain on Measured Tissue Properties," J. Biomech., 42(9), pp. 1360-1362.
80. Gefen, A., Gefen, N., Zhu, Q., Raghupathi, R., and Margulies, S. S., 2003, "Age-Dependent Changes in Material Properties of the Brain and Braincase of the Rat," J. Neurotrauma, 20(11), pp. 1163-1177. (Pubitemid 37467280)
81. Nicolle, S., Vezin, P., and Palierne, J. F., 2010, "A Strain-Hardening Bi-Power Law for the Nonlinear Behaviour of Biological Soft Tissues," J. Biomech., 43(5), pp. 927-932.
82. Freed, A. D., and Diethelm, K., 2006, "Fractional Calculus in Biomechanics: A 3D Viscoelastic Model Using Regularized Fractional Derivative Kernels With Application to the Human Calcaneal Fat Pad," Biomech. Model. Mechanobiol., 5(4), pp. 203-215. (Pubitemid 44618436)
83. Provenzano, P., Lakes, R., Keenan, T., and Vanderby, Jr., R., 2001, "Nonlinear Ligament Viscoelasticity," Ann. Biomed. Eng., 29, pp. 908-914. (Pubitemid 33147207)
84. Lakes, R. S., and Vanderby, R., 1999, "Interrelation of Creep and Relaxation: A Modeling Approach for Ligaments," J. Biomech. Eng., 121(6), pp. 612.