The connective tissue components of optic nerve head cupping in monkey experimental glaucoma part 1: Global change

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 13, 2015, Pages 7661-7678

  Yang, Hongli ^a,b   Ren, Ruojin ^a,b   Lockwood, Howard ^a,b   Williams, Galen ^a,b   Libertiaux, Vincent ^c   Downs, Crawford ^c   Gardiner, Stuart K ^b   Burgoyne, Claude F ^a,b  

^a DEVERS EYE INSTITUTE   (United States)

^b DEVERS EYE INSTITUTE   (United States)

^c UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

Glaucoma; Lamina cribrosa position and thickness; Neural canal; Optic nerve head; Peripapillary scleral position and thickness; Post BMO total prelaminar volume

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; CONFOCAL LASER MICROSCOPY; FEMALE; GLAUCOMA; IMAGE RECONSTRUCTION; INTRAOCULAR PRESSURE; MALE; MORPHOMETRICS; NONHUMAN; OPTIC NERVE DISEASE; OPTIC NERVE HEAD CUPPING; PRIORITY JOURNAL; RETINAL THICKNESS; RETROSPECTIVE STUDY; RHESUS MONKEY; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; YOUNG ADULT; ANATOMY AND HISTOLOGY; ANIMAL; CONNECTIVE TISSUE; DISEASE MODEL; IMAGE PROCESSING; MACACA FASCICULARIS; OPTIC DISK; PATHOLOGY; PATHOPHYSIOLOGY; SCLERA;

ANIMALS; CONNECTIVE TISSUE; DISEASE MODELS, ANIMAL; GLAUCOMA; IMAGE PROCESSING, COMPUTER-ASSISTED; INTRAOCULAR PRESSURE; MACACA FASCICULARIS; MACACA MULATTA; OPTIC DISK; OPTIC NERVE DISEASES; RETROSPECTIVE STUDIES; SCLERA;

EID: 84950341743     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-17624     Document Type: Article

References (64)

1. Kalvin NH, Hamasaki DI, Gass JD. Experimental glaucoma in monkeys. I. Relationship between intraocular pressure and cupping of the optic disc and cavernous atrophy of the optic nerve. Arch Ophthalmol. 1966;76:82-93.
2. Quigley HA, Addicks EM. Chronic experimental glaucoma in primates. II. Effect of extended intraocular pressure elevation on optic nerve head and axonal transport. Invest Ophthalmol Vis Sci. 1980;19:137-152.
3. Furuyoshi N, Furuyoshi M, May CA, et al. Vascular and glial changes in the retrolaminar optic nerve in glaucomatous monkey eyes. Ophthalmologica. 2000;214:24-32.
4. Jonas JB, Hayreh SS, Yong T. Thickness of the lamina cribrosa and peripapillary sclera in Rhesus monkeys with nonglaucom- atous or glaucomatous optic neuropathy. Acta Ophthalmol. 2011;89:e423-e427.
5. Burgoyne CF, Downs JC, Bellezza AJ, et al. 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.
6. Yang H, Downs JC, Girkin C, et al. 3-D histomorphometry of the normal and early glaucomatous monkey optic nerve head: lamina cribrosa and peripapillary scleral position and thickness. Invest Ophthalmol Vis Sci. 2007;48:4597-4607.
7. Yang H, Downs JC, Bellezza A, et al. 3-D histomorphometry of the normal and early glaucomatous monkey optic nerve head: prelaminar neural tissues and cupping. Invest Ophthalmol Vis Sci. 2007;48:5068-5084.
8. 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;48:3195-208.
9. 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.
10. Burgoyne CF. A biomechanical paradigm for axonal insult within the optic nerve head in aging and glaucoma. Exp Eye Res. 2011;93:120-132.
11. Roberts MD, Grau V, Grimm J, et al. Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2009;50:681-690.
12. Hernandez MR. The optic nerve head in glaucoma: role of astrocytes in tissue remodeling. Prog Retin Eye Res. 2000;19: 297-321.
13. Downs JC, Roberts MD, Sigal IA. Glaucomatous cupping of the lamina cribrosa: a review of the evidence for active progressive remodeling as a mechanism. Exp Eye Res. 2011; 93:133-140.
14. Yang H, Downs JC, Burgoyne CF. Physiologic intereye differences in monkey optic nerve head architecture and their relation to changes in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2009;50:224-234.
15. Grytz R, Girkin CA, Libertiaux V, et al. Perspectives on biomechanical growth and remodeling mechanisms in glaucoma. Mech Res Commun. 2012;42:92-106.
16. Lee EJ, Kim TW, Kim M, et al. Recent structural alteration of the peripheral lamina cribrosa near the location of disc hemorrhage in glaucoma. Invest Ophthalmol Vis Sci. 2014;55: 2805-2815.
17. Lee KM, Kim TW, Weinreb RN, et al. Anterior lamina cribrosa insertion in primary open-angle glaucoma patients and healthy subjects. PLoS One. 2014;9:e114935.
18. Burgoyne CF, Downs JC. Premise and prediction-how optic nerve head biomechanics underlies the susceptibility and clinical behavior of the aged optic nerve head. J Glaucoma. 2008;17:318-328.
19. Ren R, Yang H, Gardiner SK, et al. Anterior lamina cribrosa surface depth, age, and visual field sensitivity in the Portland Progression Project. Invest Ophthalmol Vis Sci. 2014;55: 1531-1539.
20. Burgoyne C. The morphological difference between glaucoma and other optic neuropathies. J Neuroophthalmol. 2015; 35(suppl 1):S8-S21.
21. Morgan JE. Optic nerve head structure in glaucoma: astrocytes as mediators of axonal damage. Eye. 2000;14(pt 3B):437-444.
22. Heickell AG, Bellezza AJ, Thompson HW, et al. Optic disc surface compliance testing using confocal scanning laser tomography in the normal monkey eye. J Glaucoma. 2001; 10:369-382.
23. Burgoyne CF, Downs JC, Bellezza AJ, et al. Three-dimensional reconstruction of normal and early glaucoma monkey optic nerve head connective tissues. Invest Ophthalmol Vis Sci. 2004;45:4388-4399.
24. Yang H, Thompson H, Roberts MD, et al. Deformation of the early glaucomatous monkey optic nerve head connective tissue after acute IOP elevation in 3-D histomorphometric reconstructions. Invest Ophthalmol Vis Sci. 2011;52:345-363.
25. He L, Yang H, Gardiner SK, et al. Longitudinal detection of optic nerve head changes by spectral domain optical coherence tomography in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2014;55:574-586.
26. Strouthidis NG, Yang H, Reynaud JF, et al. Comparison of clinical and spectral domain optical coherence tomography optic disc margin anatomy. Invest Ophthalmol Vis Sci. 2009; 50:4709-4718.
27. Burgoyne CF. The non-human primate experimental glaucoma model [published online ahead of print June 9, 2015]. Exp Eye Res. doi:10.1016/j.exer.2015.06.005.
28. Strouthidis NG, Yang H, Downs JC, et al. Comparison of clinical and three-dimensional histomorphometric optic disc margin anatomy. Invest Ophthalmol Vis Sci. 2009;50:2165-2174.
29. Lockwood H, Reynaud J, Gardiner S, et al. Lamina cribrosa microarchitecture in normal monkey eyes part 1: methods and initial results. Invest Ophthalmol Vis Sci. 2015;56:1618-1637.
30. Rosner B. 12.9. The intraclass correlation coefficient. In: Rosner B, ed. Fundamentals of Biostatistics. Boston, MA: Harvard University, Brooks/Cole Cengage Learning; 2011:569.
31. Gardiner SK, Fortune B, Wang L, et al. Intraocular pressure magnitude and variability as predictors of rates of structural change in non-human primate experimental glaucoma. Exp Eye Res. 2012;103:8.
32. Reynaud J, Cull G, Wang L, et al. Automated quantification of optic nerve axons in primate glaucomatous and normal eyes-method and comparison to semi-automated manual quantification. Invest Ophthalmol Vis Sci. 2012;53:2951-2959.
33. Grytz R, Sigal IA, Ruberti JW, et al. Lamina cribrosa thickening in early glaucoma predicted by a microstructure motivated growth and remodeling approach. Mech Mater. 2012;44:99-109.
34. Tatham AJ, Miki A, Weinreb RN, et al. Defects of the lamina cribrosa in eyes with localized retinal nerve fiber layer loss. Ophthalmology. 2014;121:110-118.
35. Faridi OS, Park SC, Kabadi R, et al. Effect of focal lamina cribrosa defect on glaucomatous visual field progression. Ophthalmology. 2014;121:1524-1530.
36. You JY, Park SC, Su D, et al. Focal lamina cribrosa defects associated with glaucomatous rim thinning and acquired pits. JAMA Ophthalmol. 2013;131:314-320.
37. Yang D, Fu J, Hou R, et al. Optic neuropathy induced by experimentally reduced cerebrospinal fluid pressure in monkeys. Invest Ophthalmol Vis Sci. 2014;55:3067-3073.
38. Downs JC, Burgoyne CF, Seigfreid WP, et al. 24-hour IOP telemetry in the nonhuman primate: implant system perfor- mance and initial characterization of IOP at multiple time- scales. Invest Ophthalmol Vis Sci. 2011;52:7365-7375.
39. Girard MJ, Suh JK, Bottlang M, et al. Scleral biomechanics in the aging monkey eye. Invest Ophthalmol Vis Sci. 2009;50: 5226-5237.
40. Coudrillier B, Tian J, Alexander S, et al. Biomechanics of the human posterior sclera: age-and glaucoma-related changes measured using inflation testing. Invest Ophthalmol Vis Sci. 2012;53:1714-1728.
41. Fazio MA, Grytz R, Morris JS, et al. Age-related changes in human peripapillary scleral strain. Biomech Model Mechano biol. 2014;13:551-563.
42. Yang H, He L, Gardiner SK, et al. Age-related differences in longitudinal structural change by spectral-domain optical coherence tomography in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2014;55:6409-6420.
43. Fazio MA, Grytz R, Morris JS, et al. Human scleral structural stiffness increases more rapidly with age in donors of African descent compared to donors of European descent. Invest Ophthalmol Vis Sci. 2014;55:7189-7198.
44. Sigal IA, Flanagan JG, Tertinegg I, et al. Modeling individual-specific human optic nerve head biomechanics. Part I: IOP-induced deformations and influence of geometry. Biomech Model Mechanobiol. 2009;8:85-98.
45. Sigal IA, Flanagan JG, Tertinegg I, et al. Modeling individual-specific human optic nerve head biomechanics. Part II: influence of material properties. Biomech Model Mechano-biol. 2009;8:99-109.
46. Bellezza AJ, Hart RT, Burgoyne CF. The optic nerve head as a biomechanical structure: initial finite element modeling. Invest Ophthalmol Vis Sci. 2000;41:2991-3000.
47. Clark AF. The cell and molecular biology of glaucoma: biomechanical factors in glaucoma. Invest Ophthalmol Vis Sci. 2012;53:2473-2475.
48. Teng Y, Yu X, Teng Y, et al. Evaluation of crowded optic nerve head and small scleral canal in intrapapillary hemorrhage with adjacent peripapillary subretinal hemorrhage. Graefes Arch Clin Exp Ophthalmol. 2014;252:241-248.
49. Floyd MS, Katz BJ, Digre KB. Measurement of the scleral canal using optical coherence tomography in patients with optic nerve drusen. Am J Ophthalmol. 2005;139:664-669.
50. Lee MS. Scleral canal size in patients with optic nerve drusen. Am J Ophthalmol. 2005;140:1168-1169, author reply 1169.
51. Girard MJ, Tun TA, Husain R, et al. Lamina cribrosa visibility using optical coherence tomography: comparison of devices and effects of image enhancement techniques. Invest Ophthalmol Vis Sci. 2015;56:865-874.
52. Johnson EC, Doser T, Cepurna WO, et al. Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma. Invest Ophthalmol Vis Sci. 2011;52:504-518.
53. Howell GR, Macalinao DG, Sousa GL, et al. Molecular clustering identifies complement and endothelin induction as early events in a mouse model of glaucoma. J Clin Invest. 2011;121:1429-1444.
54. Tezel G, Yang X, Luo C, et al. An astrocyte-specific proteomic approach to inflammatory responses in experimental rat glaucoma. Invest Ophthalmol Vis Sci. 2012;53:4220-4233.
55. Tezel G. A proteomics view of the molecular mechanisms and biomarkers of glaucomatous neurodegeneration. Prog Retin Eye Res. 2013;35:18-43.
56. Johnstone J, Fazio M, Rojananuangnit K, et al. Variation of the axial location of Bruch’s membrane opening with age, choroidal thickness, and race. Invest Ophthalmol Vis Sci. 2014;55:2004-2009.
57. Yang H, Downs JC, Sigal IA, et al. Deformation of the normal monkey optic nerve head connective tissue after acute IOP elevation within 3-D histomorphometric reconstructions. Invest Ophthalmol Vis Sci. 2009;50:5785-5799.
58. Downs JC, Blidner RA, Bellezza AJ, et al. Peripapillary sclera thickness in perfusion-fixed normal monkey eyes. Invest Ophthalmol Vis Sci. 2002;43:2229-2235.
59. Sommer A, Tielsch JM, Katz J, et al. Relationship between intraocular pressure and primary open angle glaucoma among white and black Americans. The Baltimore Eye Survey. Arch Ophthalmol. 1991;109:1090-1095.
60. Iwase A, Suzuki Y, Araie M, et al. The prevalence of primary open-angle glaucoma in Japanese: the Tajimi Study. Ophthalmology. 2004;111:1641-1648.
61. Leske MC, Heijl A, Hyman L, et al. Early Manifest Glaucoma Trial: design and baseline data. Ophthalmology. 1999;106: 2144-2153.
62. Gordon MO, Kass MA. The Ocular Hypertension Treatment Study: design and baseline description of the participants. Arch Ophthalmol. 1999;117:573-583.
63. Ringner M. What is principal component analysis? Nat Biotechnol. 2008;26:303-304.
64. Hata M, Miyamoto K, Oishi A, et al. Comparison of optic disc morphology of optic nerve atrophy between compressive optic neuropathy and glaucomatous optic neuropathy. PLoS One. 2014;9:e112403.