The morphological difference between glaucoma and other optic neuropathies

Journal of Neuro-Ophthalmology

Volumn 35, Issue , 2015, Pages S8-S21

  Burgoyne, Claude ^a  

^a DEVERS EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AXON; BIOMECHANICS; COMPRESSION; CONNECTIVE TISSUE; GLAUCOMA; HUMAN; INTRAOCULAR PRESSURE; NONHUMAN; OPTIC NERVE; OPTIC NERVE DISEASE; PHENOTYPE; PRIORITY JOURNAL; RETINA GANGLION CELL; RETINA MACULA LUTEA; RETINAL NERVE FIBER LAYER THICKNESS; SCLERA; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; ANIMAL; OPTIC DISK; OPTICAL COHERENCE TOMOGRAPHY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BIOMECHANICAL PHENOMENA; CONNECTIVE TISSUE; GLAUCOMA; HUMANS; OPTIC DISK; OPTIC NERVE DISEASES; RETINAL GANGLION CELLS; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84988849658     PISSN: 10708022     EISSN: 15365166     Source Type: Journal    
DOI: 10.1097/WNO.0000000000000289     Document Type: Article

References (87)

1. Van Buskirk E.M., Cioffi GA Glaucomatous optic neuropathy. Am J Ophthalmol. 1992; 113:447-452.
2. Asai T, Katsumori N, Mizokami K. Retinal ganglion cell damage in human glaucoma. 2. Studies on damage pattern [in Japanese]. Nihon Ganka Gakkai Zasshi. 1987; 91:1204-1213.
3. Garcia-Valenzuela E., Shareef S, Walsh J., Sharma SC. Programmed cell death of retinal ganglion cells during experimental glaucoma. Exp Eye Res. 1995; 61:33-44.
4. Quigley HA, Nickells RW, Kerrigan L.A., 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.
5. Janssen P, Naskar R, Moore S., Thanos S, Thiel HJ. Evidence for glaucoma-induced horizontal cell alterations in the human retina. Ger J Ophthalmol. 1996; 5:378-385.
6. Quigley HA, McKinnon SJ, Zack D.J., Pease ME, Kerrigan-Baumrind LA, Kerrigan DF, Mitchell RS Retrograde axonal transport of BDNF in retinal ganglion cells is blocked by acute IOP elevation in rats. Invest Ophthalmol Vis Sci. 2000; 41:3460-3466.
7. Nork TM, Ver Hoeve JN, Poulsen GL, Nickells RW, Davis MD, Weber A.J., Vaegan, Sarks SH, Lemley HL, Millecchia LL. Swelling and loss of photoreceptors in chronic human and experimental glaucomas. Arch Ophthalmol. 2000; 118:235-245.
8. Kendell KR, Quigley HA, Kerrigan L.A., Pease ME, Quigley EN. Primary open-angle glaucoma is not associated with photoreceptor loss. Invest Ophthalmol Vis Sci. 1995; 36:200-205.
9. Panda S, Jonas JB Decreased photoreceptor count in human eyes with secondary angle-closure glaucoma. Invest Ophthalmol Vis Sci. 1992; 33:2532-2536.
10. Weber AJ, Kaufman PL, Hubbard WC Morphology of single ganglion cells in the glaucomatous primate retina. Invest Ophthalmol Vis Sci. 1998; 39:2304-2320.
11. Wygnanski T, Desatnik H, Quigley H.A., Glovinsky Y. Comparison of ganglion cell loss and cone loss in experimental glaucoma. Am J Ophthalmol. 1995; 120:184-189.
12. Crish SD, Sappington RM, Inman D.M., Horner PJ, Calkins DJ. Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proc Natl Acad Sci U S A. 2010; 107:5196-5201.
13. Crish SD, Dapper JD, MacNamee S.E., Balaram P., Sidorova TN, Lambert WS, Calkins DJ. Failure of axonal transport induces a spatially coincident increase in astrocyte BDNF prior to synapse loss in a central target. Neuroscience. 2013; 229: 55-70.
14. Yucel YH, Zhang Q, Gupta N., Kaufman PL, Weinreb RN. Loss of neurons in magnocellular and parvocellular layers of the lateral geniculate nucleus in glaucoma. Arch Ophthalmol. 2000; 118:378-384.
15. Yucel YH, Zhang Q, Weinreb R.N., Kaufman PL, Gupta N. Atrophy of relay neurons in magno- and parvocellular layers in the lateral geniculate nucleus in experimental glaucoma. Invest Ophthalmol Vis Sci. 2001; 42:3216-3222.
16. Yucel YH, Zhang Q, Weinreb R.N., Kaufman PL, Gupta N. Effects of retinal ganglion cell loss on magno-, parvo-, koniocellular pathways in the lateral geniculate nucleus and visual cortex in glaucoma. Prog Retin Eye Res. 2003; 22:465-481.
17. Vrabec F. Glaucomatous cupping of the human optic disk: a neuro-histologic study. Albrecht Von Graefes Arch Klin Exp Ophthalmol. 1976; 198:223-234.
18. Bellezza AJ, Rintalan CJ, Thompson H.W., Downs JC, Hart RT, Burgoyne CF. Deformation of the lamina cribrosa and anterior scleral canal wall in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2003; 44:623-637.
19. Burgoyne CF, Downs JC, Bellezza A.J., Hart RT. Three-dimensional reconstruction of normal and early glaucoma monkey optic nerve head connective tissues. Invest Ophthalmol Vis Sci. 2004; 45:4388-4399.
20. Quigley HA, Guy J, Anderson DR Blockade of rapid axonal transport. Effect of intraocular pressure elevation in primate optic nerve. Arch Ophthalmol. 1979; 97:525-531.
21. Quigley HA, Addicks EM, Green W.R., Maumenee AE. Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage. Arch Ophthalmol. 1981; 99:635-649.
22. Minckler DS, Bunt AH, Johanson GW Orthograde and retrograde axoplasmic transport during acute ocular hypertension in the monkey. Invest Ophthalmol Vis Sci. 1977; 16:426-441.
23. Gaasterland D, Tanishima T, Kuwabara T. Axoplasmic flow during chronic experimental glaucoma. 1. Light and electron microscopic studies of the monkey optic nervehead during development of glaucomatous cupping. Invest Ophthalmol Vis Sci. 1978; 17:838-846.
24. Downs JC, Suh JK, Thomas K.A., 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.
25. Downs JC, Yang H, Girkin C., Sakata L, Bellezza A, Thompson H., Burgoyne CF 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.
26. Yang H, Downs JC, Girkin C, Sakata L., Bellezza A, Thompson H, Burgoyne CF 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.
27. Yang H, Downs JC, Bellezza A, Thompson H., Burgoyne CF. 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.
28. Johnson EC, Deppmeier LM, Wentzien S.K., Hsu I., Morrison JC. Chronology of optic nerve head and retinal responses to elevated intraocular pressure. Invest Ophthalmol Vis Sci. 2000; 41:431-442.
29. Johnson EC, Morrison JC, Farrell S, Deppmeier L., Moore CG, McGinty MR. The effect of chronically elevated intraocular pressure on the rat optic nerve head extracellular matrix. Exp Eye Res. 1996; 62:663-674.
30. Danias J, Lee KC, Zamora M.F., Chen B., Shen F, Filippopoulos T, Su Y., Goldblum D, Podos SM, Mittag T. Quantitative analysis of retinal ganglion cell (RGC) loss in aging DBA/2NNia glaucomatous mice: comparison with RGC loss in aging C57/BL6 mice. Invest Ophthalmol Vis Sci. 2003; 44:5151-5162.
31. Filippopoulos T, Danias J, Chen B., Podos SM, Mittag TW. Topographic and morphologic analyses of retinal ganglion cell loss in old DBA/2NNia mice. Invest Ophthalmol Vis Sci. 2006; 47:1968-1974.
32. Howell GR, Libby RT, Jakobs T.C., Smith RS, Phalan FC, Barter JW, Barbay J.M., Marchant JK, Mahesh N, Porciatti V, Whitmore A.V., Masland RH, John SW. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J Cell Biol. 2007; 179:1523-1537.
33. Jakobs TC, Libby RT, Ben Y, John S.W., Masland RH. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J Cell Biol. 2005; 171:313-325.
34. Schlamp CL, Li Y, Dietz J.A., Janssen KT, Nickells RW. Progressive ganglion cell loss and optic nerve degeneration in DBA/2J mice is variable and asymmetric. BMC Neurosci. 2006; 7:66.
35. Langham M. The temporal relation between intraocular pressure and loss of vision in chronic simple glaucoma. Glaucoma. 1980; 2:427-435.
36. Anderson DR, Hoyt WF Ultrastructure of intraorbital portion of human and monkey optic nerve. Arch Ophthalmol. 1969; 82:506-530.
37. 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.
38. Cioffi GA, Van Buskirk EM. Vasculature of the anterior optic nerve and peripapillary choroid. In: Ritch R, Shields MB, Krupin T, eds. The Glaucomas. St. Louis, MO: Mosby; 1996:177-197.
39. Quigley HA. Overview and introduction to session on connective tissue of the optic nerve in glaucoma. Chapter 2. In: Drance SM, Anderson DR, eds. Optic Nerve in Glaucoma. Amsterdam, NY: Kugler Publications; 1995:15-36.
40. Quigley HA, Brown AE, Morrison J.D., Drance SM. The size and shape of the optic disc in normal human eyes. Arch Ophthalmol. 1990; 108:51-57.
41. Morrison JC, L'Hernault NL, Jerdan JA, Quigley HA Ultrastructural location of extracellular matrix components in the optic nerve head. Arch Ophthalmol. 1989; 107:123-129.
42. Anderson DR. Ultrastructure of human and monkey lamina cribrosa and optic nerve head. Arch Ophthalmol. 1969; 82:800-814.
43. Nicolela MT, Drance SM Various glaucomatous optic nerve appearances: clinical correlations. Ophthalmology. 1996; 103:640-649.
44. Nicolela MT, McCormick TA, Drance S.M., Ferrier SN, LeBlanc RP, Chauhan BC. Visual field and optic disc progression in patients with different types of optic disc damage: a longitudinal prospective study. Ophthalmology. 2003; 110:2178-2184.
45. Burgoyne CF, Downs JC, Bellezza A.J., 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.
46. Burgoyne CF. A biomechanical paradigm for axonal insult within the optic nerve head in aging and glaucoma. Exp Eye Res. 2011; 93:120-132.
47. Yang H, Williams G, Downs J.C., Sigal IA, Roberts MD, Thompson H, Burgoyne CF Posterior (outward) migration of the lamina cribrosa and early cupping in monkey experimental glaucoma. Invest Ophthalmol Vis Sci. 2011; 52:7109-7121.
48. Roberts MD, Grau V, Grimm J., Reynaud J, Bellezza AJ, Burgoyne C.F., Downs JC Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2009; 50:681-690.
49. Burgoyne CF, Morrison JC The anatomy and pathophysiology of the optic nerve head in glaucoma. J Glaucoma. 2001; 10: S16-S18.
50. Sigal IA, Ethier CR Biomechanics of the optic nerve head. Exp Eye Res. 2009; 88:799-807.
51. Sigal IA, Flanagan JG, Tertinegg I, Ethier CR Modeling individual-specific human optic nerve head biomechanics. Part II: influence of material properties. Biomech Model Mechanobiol. 2009; 8:99-109.
52. Sigal IA, Flanagan JG, Tertinegg I, Ethier CR Modeling individual-specific human optic nerve head biomechanics. Part I: IOP-induced deformations and influence of geometry. Biomech Model Mechanobiol. 2009; 8:85-98.
53. Sigal IA. Interactions between geometry and mechanical properties on the optic nerve head. Invest Ophthalmol Vis Sci. 2009; 50:2785-2795.
54. Morgan WH, Yu DY, Alder V.A., Cringle SJ, Cooper RL, House PH, Constable IJ The correlation between cerebrospinal fluid pressure and retrolaminar tissue pressure. Invest Ophthalmol Vis Sci. 1998; 39:1419-1428.
55. Downs JC, Roberts MD, Burgoyne CF Mechanical strain and restructuring of the optic nerve head. In: Shaarawy T, Sherwood MB, Hitchings RA, Crowston JG, eds. Glaucoma. London, United Kingdom: Saunders; 2009.
56. Bellezza AJ, Rintalan CJ, Thompson H.W., Downs JC, Hart RT, Burgoyne CF. Anterior scleral canal geometry in pressurised (IOP 10) and non-pressurised (IOP 0) normal monkey eyes. Br J Ophthalmol. 2003; 87:1284-1290.
57. Sigal IA, Flanagan JG, Ethier CR Factors influencing optic nerve head biomechanics. Invest Ophthalmol Vis Sci. 2005; 46:4189-4199.
58. Morgan WH, Chauhan BC, Yu D.Y., Cringle SJ, Alder VA, House PH. Optic disc movement with variations in intraocular and cerebrospinal fluid pressure. Invest Ophthalmol Vis Sci. 2002; 43:3236-3242.
59. Yang H, Downs JC, Sigal I.A., Roberts MD, Thompson H, Burgoyne CF. 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.
60. Qin L, Yang H, Williams G., Gardiner S, Downs JC, Fortune B, Burgoyne CF IOVS. 2012; 53: ARVO E-Abstract 2824.
61. Agoumi Y, Sharpe GP, Hutchison D.M., Nicolela MT, Artes PH, Chauhan BC. Laminar and prelaminar tissue displacement during intraocular pressure elevation in glaucoma patients and healthy controls. Ophthalmology. 2011; 118:52-59.
62. Morgan WH, Yu DY, Balaratnasingam C. The role of cerebrospinal fluid pressure in glaucoma pathophysiology: the dark side of the optic disc. J Glaucoma. 2008; 17:408-413.
63. Jonas JB. Trans-lamina cribrosa pressure difference. Arch Ophthalmol. 2007; 125:431; author reply 431.
64. Jonas JB, Berenshtein E, Holbach L. Lamina cribrosa thickness and spatial relationships between intraocular space and cerebrospinal fluid space in highly myopic eyes. Invest Ophthalmol Vis Sci. 2004; 45:2660-2665.
65. Jonas JB, Berenshtein E, Holbach L. Anatomic relationship between lamina cribrosa, intraocular space, and cerebrospinal fluid space. Invest Ophthalmol Vis Sci. 2003; 44:5189-5195.
66. Yang H, He L, Gardiner S.K., Reynaud J., Williams G, Hardin C, Strouthidis N.G., Downs JC, Fortune B, Burgoyne CF Age-related differences in longitudinal structural change by spectraldomain optical coherence tomography in early experimental glaucoma. Invest Ophthalmol Vis Sci. 2014; 55:6409-6420.
67. 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.
68. He L, Yang H, Gardiner S.K., Williams G., Hardin C, Strouthidis NG, Fortune B, Burgoyne CF 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.
69. Nguyen JV, Soto I, Kim K.Y., Bushong EA, Oglesby E, Valiente-Soriano FJ, Yang Z, Davis C.H., Bedont JL, Son JL, Wei JO, Buchman V.L., Zack DJ, Vidal-Sanz M, Ellisman MH, Marsh-Armstrong N. Myelination transition zone astrocytes are constitutively phagocytic and have synuclein dependent reactivity in glaucoma. Proc Natl Acad Sci U S A. 2011; 108:1176-1181.
70. Davis CH, Kim KY, Bushong E.A., Mills EA, Boassa D, Shih T, Kinebuchi M., Phan S, Zhou Y, Bihlmeyer N.A., Nguyen JV, Jin Y, Ellisman MH, Marsh-Armstrong N. Transcellular degradation of axonal mitochondria. Proc Natl Acad Sci U S A. 2014; 111:9633-9638.
71. Sigal IA, Flanagan JG, Tertinegg I, Ethier CR 3D morphometry of the human optic nerve head. Exp Eye Res. 2010; 90:70-80.
72. Ivers K, Ing E, Yang H., Gardiner SK, Reynaud J, Cull G, Wang L., Burgoyne CF Lamina cribrosa position in the monkey optic nerve transection model of a non-glaucomatous optic neuropathy. AGS Meeting Abstract 2015; Accepted for presentation.
73. Helb HM, Charbel Issa P, Fleckenstein M, Schmitz-Valckenberg S, Scholl H.P., Meyer CH, Eter N, Holz FG Clinical evaluation of simultaneous confocal scanning laser ophthalmoscopy imaging combined with high-resolution, spectral-domain optical coherence tomography. Acta Ophthalmol. 2010; 88:842-849.
74. He L, Ren R, Yang H., Hardin C, Reyes L, Reynaud J., Gardiner SK, Fortune B, Demirel S, Burgoyne CF Anatomic vs. acquired image frame discordance in spectral domain optical coherence tomography minimum rim measurements. PLoS One. 2014; 9:e92225.
75. Strouthidis NG, Fortune B, Yang H., Sigal IA, Burgoyne CF. Longitudinal change detected by spectral domain optical coherence tomography in the optic nerve head and peripapillary retina in experimental glaucoma. Invest Ophthalmol Vis Sci. 2011; 52:1206-1219.
76. Ren R, Yang H, Gardiner S.K., Fortune B., Hardin C, Demirel S, Burgoyne CF Anterior lamina cribrosa surface depth, age, and visual field sensitivity in the Portland Progression Project. Invest Ophthalmol Vis Sci. 2014; 55:1531-1539.
77. Gardiner SK, Ren R, Yang H., Fortune B, Burgoyne CF, Demirel S. A method to estimate the amount of neuroretinal rim tissue in glaucoma: comparison with current methods for measuring rim area. Am J Ophthalmol. 2014; 157:540-549 e541-542.
78. Hosseini H, Nassiri N, Azarbod P., Giaconi J, Chou T, Caprioli J., Nouri-Mahdavi K. Measurement of the optic disc vertical tilt angle with spectral-domain optical coherence tomography and influencing factors. Am J Ophthalmol. 2013; 156:737-744.
79. Lamparter J, Russell RA, Zhu H, Asaoka R., Yamashita T, Ho T, Garway-Heath DF. The influence of intersubject variability in ocular anatomical variables on the mapping of retinal locations to the retinal nerve fiber layer and optic nerve head. Invest Ophthalmol Vis Sci. 2013; 54:6074-6082.
80. Strouthidis NG, Yang H, Reynaud J.F., Grimm JL, Gardiner SK, Fortune B, Burgoyne CF Comparison of clinical and spectral domain optical coherence tomography optic disc margin anatomy. Invest Ophthalmol Vis Sci. 2009; 50:4709-4718.
81. Chen CS, Johnson MA, Flower R.A., Slater BJ, Miller NR, Bernstein SL. A primate model of nonarteritic anterior ischemic optic neuropathy. Invest Ophthalmol Vis Sci. 2008; 49: 2985-2992.
82. Miller NR, Johnson MA, Nolan T, Guo Y., Bernstein AM, Bernstein SL. Sustained neuroprotection from a single intravitreal injection of PGJ2 in a non-human primate model of nonarteritic anterior ischemic optic neuropathy. Invest Ophthalmol Vis Sci. 2014; 55:7047-7056.
83. Yang D, Fu J, Hou R., Liu K, Jonas JB, Wang H, Chen W., Li Z, Sang J, Zhang Z., Liu S, Cao Y, Xie X., Ren R, Lu Q, Weinreb R.N., Wang N. Optic neuropathy induced by experimentally reduced cerebrospinal fluid pressure in monkeys. Invest Ophthalmol Vis Sci. 2014; 55:3067-3073.
84. Reis AS, Sharpe GP, Yang H, Nicolela M.T., Burgoyne CF, Chauhan BC. Optic disc margin anatomy in patients with glaucoma and normal controls with spectral domain optical coherence tomography. Ophthalmology. 2012; 119:738-747.
85. Reis AS, O'Leary N, Yang H, Sharpe G.P., Nicolela MT, Burgoyne CF, Chauhan BC Influence of clinically invisible, but optical coherence tomography detected, optic disc margin anatomy on neuroretinal rim evaluation. Invest Ophthalmol Vis Sci. 2012; 53:1852-1860.
86. Chauhan BC, O'Leary N, Almobarak FA, Reis A.S., Yang H., Sharpe GP, Hutchison DM, Nicolela MT, Burgoyne CF Enhanced detection of open-angle glaucoma with an anatomically accurate optical coherence tomography-derived neuroretinal rim parameter. Ophthalmology. 2013; 120: 535-543.
87. Chauhan BC, Burgoyne CF From clinical examination of the optic disc to clinical assessment of the optic nerve head: a paradigm change. Am J Ophthalmol. 2013; 156:218-227. e212.