Studies of scleral biomechanical behavior related to susceptibility for retinal ganglion cell loss in experimental mouse glaucoma

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 3, 2013, Pages 1767-1780

  Nguyen, Cathy ^a   Cone, Frances E ^a   Nguyen, Thao D ^b   Coudrillier, Baiste ^b   Pease, Mary E ^a   Steinhart, Matthew R ^a   Oglesby, Ericka N ^a   Jefferys, Joan L ^a   Quigley, Harry A ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYSTYRENE;

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; CELL LOSS; CONTROLLED STUDY; DISEASE PREDISPOSITION; EYE AXIS LENGTH; GLAUCOMA; INTRAOCULAR PRESSURE; MOUSE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; RETINA GANGLION CELL; SCLERA; STRESS; THICKNESS;

ANIMALS; APOPTOSIS; AXIAL LENGTH, EYE; AXONS; BIOMECHANICS; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; ELASTICITY; GLAUCOMA; INTRAOCULAR PRESSURE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; OPTIC NERVE DISEASES; RETINAL GANGLION CELLS; SCLERA; TONOMETRY, OCULAR;

EID: 84875443308     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-10952     Document Type: Article

References (75)

1. Bengtsson B, Heijl A. Diurnal IOP fluctuation: not an independent risk factor for glaucomatous visual field loss in high-risk ocular hypertension. Graefe's Arch Clin Exper Ophthalmol. 2005;243:513-518.
2. Nouri-Mahdavi K, Hoffman D, Coleman A, et al. Predictive factors for glaucomatous visual field progression in the Advanced Glaucoma Intervention Study. Ophthalmology. 2004;111:1627-1635.
3. De Moraes CG, Juthani VJ, Liebmann JM, et al. Risk factors for visual field progression in treated glaucoma. Arch Ophthalmol. 2011;129:562-568.
4. Quigley HA, Hohman RM, Addicks EM, Massof RS, Green WR. Morphologic changes in the lamina cribrosa correlated with neural loss in open-angle glaucoma. Am J Ophthalmol. 1983; 95:673-691.
5. Danesh-Meyer HV, Boland MV, Savino PJ, et al. Optic disc morphology in open angle glaucoma compared with anterior ischemic optic neuropathies. Invest Ophthalmol Vis Sci. 2010; 51:2003-2010.
6. Kerrigan LA, Zack DJ, Quigley HA, Smith SD, Pease ME. TUNEL-positive ganglion cells in human primary open angle glaucoma. Arch Ophthalmol. 1997;115:1031-1035.
7. Quigley HA, Nickells RW, Kerrigan LA, Pease ME, Thibault DJ, Zack DJ. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci. 1995;36:774-786.
8. Quigley HA, Addicks EM. Regional differences in the structure of the lamina cribrosa and their relation to glaucomatous optic nerve damage. Arch Ophthalmol. 1981;99:137-143.
9. Dandona L, Quigley HA, Brown AE, Enger C. Quantitative regional structure of the normal human lamina cribrosa. A racial comparison. Arch Ophthalmol. 1990;108:393-398.
10. Quigley HA, Green WR. The histology of human glaucoma cupping and optic nerve damage: clinicopathologic correlation in 21 eyes. Ophthalmology. 1979;10:1803-1827.
11. Quigley HA, Addicks EM, Green WR, Maumenee AE. Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage. Arch Ophthalmol. 1981;99:635-649.
12. Quigley HA, Addicks EM, Green WR. Optic nerve damage in human glaucoma. III. Quantitative correlation of nerve fiber loss and visual field defect in glaucoma, ischemic neuropathy, disc edema, and toxic neuropathy. Arch Ophthalmol. 1982; 100:135-146.
13. Boland MV, Quigley HA. Risk factors and open-angle glaucoma: concepts and applications. J Glaucoma. 2007;16:406-418.
14. Congdon NG, Broman AT, Bandeen-Roche K, Grover D, Quigley HA. Central corneal thickness and corneal hysteresis associated with glaucoma damage. Am J Ophthalmol. 2006; 141:868-875.
15. Ebneter A, Wagels B, Zinkernagel MS. Non-invasive biometric assessment of ocular rigidity in glaucoma patients and controls. Eye. 2009;23:606-611.
16. Hommer A, Fuchsjager-Mayr G, Resch H, Vass C, Garhofer G, Schmetterer L. Estimation of ocular rigidity based on measurement of pulse amplitude using pneumotonometry and fundus pulse using laser interferometry in glaucoma. Invest Ophthalmol Vis Sci. 2008;49:4046-4050.
17. Yang H, Williams G, Downs JC, et al. Posterior (outward) migration of the lamina cribrosa and early cupping in monkey experimental glaucoma. Invest Ophthalmol Vis Sci. 2011;52; 7109-7121.
18. Burgoyne CF, Downs JC, Bellezza AJ, Suh JK, Hart RT. 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 Retin Eye Res. 2005;24:39-73.
19. Sigal IA, Yang H, Roberts MD, Burgoyne CF, Downs JC. IOPinduced lamina cribrosa displacement and scleral canal expansion: an analysis of factor interactions using parameterized eye-specific models. Invest Ophthalmol Vis Sci. 2011;52: 1896-1907.
20. Sigal IA, Flanagan JG, Ethier CR. Factors influencing optic nerve head biomechanics. Invest Ophthalmol Vis Sci. 2005; 46:4189-4199.
21. Girard MJA, Suh J-KF, Mottlang M, Burgoyne CF, Downs JC. Biomechanical changes in the sclera of monkey eyes exposed to chronic IOP elevations. Invest Ophthamol Vis Sci. 2011;52: 5656-5669.
22. Quigley HA, Broman A. The number of persons with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006;90:151-156.
23. Downs JC, Suh J-KF, Thomas KA, Bellezza AJ, Hart RT, Burgoyne CF. Viscoelastic material properties of the peripapillary sclera in normal and early-glaucoma monkey eyes. Invest Ophthalmol Vis Sci. 2005;46:540-546.
24. Woo SL, Kobayashi AS, Schlegel WA, Lawrence C. Nonlinear material properties of intact cornea and sclera. Exp Eye Res. 1972;14:29-39.
25. Spoerl E, Boehm AG, Pillunat LE. The influence of various substances on the biomechanical behavior of lamina cribrosa and peripapillary sclera. Invest Ophthalmol Vis Sci. 2005;46: 1286-1290.
26. Myers KM, Cone FE, Quigley HA, Gelman SE, Pease ME, Nguyen TD. The in vitro inflation response of mouse sclera. Exp Eye Res. 2010;91:866-875.
27. Girard MJ, Suh JK, Bottlang M, Burgoyne CF, Downs JC. Scleral biomechanics in the aging monkey eye. Invest Ophthalmol Vis Sci. 2009;50:5226-5237.
28. Downs JC, Yang H, Girkin C, et al. Three-dimensional histomorphometry of the normal and early glaucomatous monkey optic nerve head: neural canal and subarachnoid space architecture. Invest Ophthalmol Vis Sci. 2007;48:3195-3208.
29. Phillips JR, Khalaj M, McBrien NA. Induced myopia associated with increased scleral creep in the chick and tree shrew eyes. Invest Ophthalmol Vis Sci. 2000;41:2028-2034.
30. Coudrillier B, Tian J, Alexander S, Myers KM, Quigley HA, Nguyen TD. Biomechanics of the human posterior sclera: age-and glaucoma-related changes measured using inflation testing. Invest Ophthalmol Vis Sci. 2012;53:1714-1728.
31. Myers KM, Coudrillier B, Boyce BL, Nguyen TD. The inflation response of the posterior bovine sclera. Acta Biomaterialia. 2010;6:4327-4335.
32. Morrison JC, Dorman-Pease ME, Dunkelberger GR, Quigley HA. Optic nerve head extracellular matrix in primary optic atrophy and experimental glaucoma. Arch Ophthalmol. 1990; 108:1020-1024.
33. Morrison JC, Moore CG, Deppmeier LMH, Gold BF, Meshul CK, Johnson EC. A rat model of chronic pressure-induced optic nerve damage. Exp Eye Res. 1997;64:85-96.
34. Morrison JC, Nylander KB, Lauer AK, Cepurna WO, Johnson E. Glaucoma drops control intraocular pressure and protect optic nerves in a rat model of glaucoma. Invest Ophthalmol Vis Sci. 1998;39:526-531.
35. Heijl A, Leske MC, Bengtsson B, et al. Reduction of intraocular pressure and glaucoma progression. Arch Ophthalmol. 2002; 120:1268-1279.
36. Sun D, Lye-Barthel M, Masland RH, Jakobs TC. The morphology and spatial arrangement of astrocytes in the optic nerve head of the mouse. J Comp Neurol. 2009;516:1-19.
37. Zhou J, Rappaport EF, Tobias JW, Young TL. Differential gene expression in mouse sclera during ocular development. Invest Ophthalmol Vis Sci. 2006;47:1794-1802.
38. Olsen TW, Aaberg SY, Geroski DH, Edelhauser HF. Human sclera: thickness and surface area. Am J Ophthalmol. 1998; 125:237-241.
39. Cone FE, Steinhart MR, Oglesby EN, Kalesnykas G, Pease ME, Quigley HA. The effects of anesthesia, mouse strain and age on intraocular pressure and an improved murine model of experimental glaucoma. Exp Eye Res. 2012;99:27-35.
40. Cone FE, Gelman SE, Son JL, Pease ME, Quigley HA. Differential susceptibility to experimental glaucoma among 3 mouse strains using bead and viscoelastic injection. Exp Eye Res. 2010;91:415-424.
41. Helm J, McNeill S, Sutton M. Three-dimensional image correlation for surface displacement measurements. Opt Eng. 1996;35:1911-1920.
42. Levkovitch-Verbin H, Quigley HA, Martin KR, Valenta D, Baumrind LA, Pease ME. Translimbal laser photocoagulation to the trabecular meshwork as a model of glaucoma in rats. Invest Ophthalmol Vis Sci. 2002;43:402-410.
43. Marina N, Bull ND, Martin KR. A semiautomated targeted sampling method to assess optic nerve axonal loss in a rat model of glaucoma. Nat Protocol. 2010;5:1642-1651.
44. Steinhart MR, Cone FE, Nguyen C, et al. Mice with an induced mutation in collagen 8A2 develop larger eyes and are resistant to retinal ganglion cell damage in an experimental glaucoma model. Mol Vis. 2012;18:1093-1106.
45. Norman RE, Flanagan JG, Rausch SM, et al. Dimensions of the human sclera: thickness measurement and regional changes with axial length. Exp Eye Res. 2010;90:277-284.
46. Hogan MJ, Alvarado JA, Weddell JE. Histology of the Human Eye. Philadelphia: W. B. Saunders Co.; 1971:193-200.
47. Hernandez MR, Luo XX, Igoe F, Neufeld AH. Extracellular matrix of the human lamina cribrosa. Am J Ophthalmol. 1987; 104:567-576.
48. Gelman S, Cone FE, Pease ME, Nguyen TD, Myers K, Quigley HA. The presence and distribution of elastin in the posterior and retrobulbar regions of the mouse eye. Exp Eye Res. 2010; 90:210-215.
49. Girard MJA, Dahlmann-Noor A, Rayapureddi S, et al. Quantitative mapping of scleral fiber orientation in normal rat eyes. Invest Ophthamol Vis Sci. 2011;52:9684-9693.
50. Girard MJ, Downs JC, Bottlang M, Burgoyne CF, Suh JK. Peripapillary and posterior scleral mechanics, II: experimental and inverse finite element characterization. J Biomech Eng. 2009;131:051012.
51. Yan D, McPheeters S, Johnson G, Utzinger U, Vande Geest JP. Microstructural differences in the human posterior sclera as a function of age and race. Invest Ophthalmol Vis Sci. 2011;52: 821-829.
52. Rada JA, Shelton S, Norton TT. The sclera and myopia. Exp Eye Res. 2006;82:185-200.
53. Pijanka JK, Coudrillier B, Ziegler K, et al. Quantitative Mapping of collagen fiber orientation in non-glaucoma and glaucoma posterior human sclerae. Invest Ophthalmol Vis Sci. 2012;53: 5258-5270.
54. Norman RE, Flanagan JG, Sigal IA, Rausch SMK, Tertinegg I, Ethier CR. Finite element modeling of the human sclera: influence on optic nerve head biomechanics and connections with glaucoma. Exp Eye Res. 2011;93:4-12.
55. Quigley HA. The pathogenesis of reversible cupping in congenital glaucoma. Am J Ophthalmol. 1977;84:358-370.
56. Martus P, Stroux A, Budde WM, Mardin CY, Korth M, Jonas JB. Predictive factors for progressive optic nerve damage in various types of chronic open-angle glaucoma. Am J Ophthalmol. 2005;139:999-1009.
57. Ren R, Wang N, Li B, et al. Lamina cribrosa and peripapillary sclera histomorphometry in normal and advanced glaucomatous Chinese eyes with various axial length. Invest Ophthalmol Vis Sci. 2009;50:2175-2184.
58. Downs JC, Ensor ME, Bellezza AJ, Thompson HW, Hart RT, Burgoyne CF. Posterior scleral thickness in perfusion-fixed normal and early-glaucoma monkey eyes. Invest Ophthalmol Vis Sci. 2001;42:3202-3208.
59. Grytz R, Girkin CA, Libertiaux V, Downs JC. Perspectives on biomechanical growth and remodeling mechanisms in glaucoma. Mech Res Commun. 2012;42:92-106.
60. Zeimer RC, Ogura Y. The relation between glaucomatous damage and optic nerve head mechanical compliance. Arch Ophthalmol. 1989;107:1232-1234.
61. Roberts MD, Sigal AI, Liang Y, Bugoyne CF, Downs JC. Changes in the biomechanical response of the optic nerve head in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2010;51: 5675-5684.
62. Hernandez MR, Andrzejewska WM, Neufeld AH. Changes in the extracellular matrix of the human optic nerve head in primary open-angle glaucoma. Am J Ophthalmol. 1990;109: 180-188.
63. Quigley HA, Dorman-Pease ME, Brown AE. Quantitative study of collagen and elastin of the optic nerve head and sclera in human and experimental monkey glaucoma. Curr Eye Res. 1991;10:877-888.
64. Quigley HA, Brown A, Dorman-Pease ME. Alterations in elastin of the optic nerve head in human and experimental glaucoma. Br J Ophthalmol. 1991;75:552-557.
65. Quigley EN, Quigley HA, Pease ME, Kerrigan LA. Quantitative studies of elastin in the optic nerve heads of persons with open-angle glaucoma. Ophthalmology. 1996;103:1680-1685.
66. Hernandez MR. Ultrastructural immunocytochemical analysis of elastin in the human lamina cribrosa. Changes in elastic fibers in primary open-angle glaucoma. Invest Ophthalmol Vis Sci. 1992;33:2891-2903.
67. Quigley HA, Pease ME, Thibault D. Change in the appearance of elastin in the lamina cribrosa of glaucomatous optic nerve heads. Graefe's Arch Clin Exp Ophthalmol. 1994;232:257-261.
68. Pena JD, Netland PA, Vidal I, Dorr DA, Rasky A, Hernandez MR. Elastosis of the lamina cribrosa in glaucomatous optic neuropathy. Exp Eye Res. 1998;67:517-524.
69. Aghamohammadzadeh H, Newton RH, Meek KM. X-ray scattering used to map the preferred collagen orientation in the human cornea and limbus. Structure. 2004;12:249-256.
70. Urban Z, Agapova O, Hucthagowder V, Yang P, Starcher BC, Hernandez MR. Population differences in elastin maturation in optic nerve head tissue and astrocytes. Invest Ophthalmol Vis Sci. 2007;48:3209-3215.
71. Thorleifsson G, Magnusson KP, Sulem P, et al. Common sequence variants in the LOXL1 gene confer susceptibility to exfoliation glaucoma. Science. 2007;317:1397-1400.
72. Netland PA, Ye H, Streeten BW, Hernandez MR. Elastosis of the lamina cribrosa in pseudoexfoliation syndrome with glaucoma. Ophthalmology. 1995;102:878-886.
73. Gottanka J, Kuhlmann A, Scholz M, Johnson DH, Lütjen-Drecoll E. Pathophysiologic changes in the optic nerves of eyes with primary open angle and pseudoexfoliation glaucoma. Invest Ophthalmol Vis Sci. 2005;46:4170-4181.
74. Yoo L, Reed J, Shin A, et al. Characterization of ocular tissues using micro-indentation and Hertzian viscoelastic models. Invest Ophthalmol Vis Sci. 2011;52:3475-3482.
75. Winkler M, Chai D, Kriling S, et al. Non-linear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics. Invest Ophthalmol Vis Sci. 2011;52: 8818-8827.