Age-related differences in longitudinal structural change by spectral-domain optical coherence tomography in early experimental glaucoma

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 10, 2014, Pages 6409-6420

  Yang, Hongli ^a,b   He, Lin ^a,b   Gardiner, Stuart K ^b   Reynaud, Juan ^a,b   Williams, Galen ^a,b   Hardin, Christy ^a,b   Strouthidis, Nicholas G ^c   Crawford Downs, J ^d   Fortune, Brad ^b   Burgoyne, Claude F ^a,b  

^a DEVERS EYE INSTITUTE   (United States)

^b DEVERS EYE INSTITUTE   (United States)

^c and University of Bristol   (United Kingdom)

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

Author keywords

BMO minimum rim width; Glaucoma; Lamina cribrosa; Optic nerve head; Optical coherence tomography

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRUCH MEMBRANE OPENING; CONNECTIVE TISSUE; CONTROLLED STUDY; EXPERIMENTAL GLAUCOMA; FOLLOW UP; IMAGE PROCESSING; IMAGE RECONSTRUCTION; INTERNAL LIMITING MEMBRANE; INTRAOCULAR PRESSURE; LASER COAGULATION; LONGITUDINAL STUDY; MINIMUM RIM WIDTH; NONHUMAN; OPTIC NERVE; OPTIC NERVE FIBER; PIGMENT EPITHELIUM; RETINAL NERVE FIBER LAYER THICKNESS; RHESUS MONKEY; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; VISUAL SYSTEM PARAMETERS; AGING; ANIMAL; DISEASE COURSE; DISEASE MODEL; GLAUCOMA; HUMAN; NERVE FIBER; OPTIC DISK; OPTICAL COHERENCE TOMOGRAPHY; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; THREE DIMENSIONAL IMAGING; TIME;

AGING; ANIMALS; AXONS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GLAUCOMA; HUMANS; IMAGING, THREE-DIMENSIONAL; INTRAOCULAR PRESSURE; MACACA MULATTA; OPTIC DISK; TIME FACTORS; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84908110006     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.14-14156     Document Type: Article

References (49)

1. Bianchi-Marzoli S, Rizzo JF III, Brancato R, Lessell S. Quantitative analysis of optic disc cupping in compressive optic neuropathy. Ophthalmology. 1995;102:436–440
2. Greenfield DS, Siatkowski RM, Glaser JS, Schatz NJ, Parrish RK II. The cupped disc. Who needs neuroimaging? Ophthalmology. 1998;105:1866–1874
3. Klein BE, Klein R, Lee KE, Hoyer CJ. Does the intraocular pressure effect on optic disc cupping differ by age? Trans Am Ophthalmol Soc. 2006;104:143–148
4. Quigley HA, Green WR. The histology of human glaucoma cupping and optic nerve damage: clinicopathologic correlation in 21 eyes. Ophthalmology. 1979;86:1803–1830
5. Quigley H, Anderson DR. Cupping of the optic disc in ischemic optic neuropathy. Trans Sect Ophthalmol Am Acad Ophthalmol Otolaryngol. 1977;83:755–762
6. Trobe JD, Glaser JS, Cassady J, Herschler J, Anderson DR. Nonglaucomatous excavation of the optic disc. Arch Ophthalmol. 1980;98:1046–1050
7. Ambati BK, Rizzo JF III. Nonglaucomatous cupping of the optic disc. Int Ophthalmol Clin. 2001;41:139–149
8. Greenfield DS. Glaucomatous versus nonglaucomatous optic disc cupping: clinical differentiation. Semin Ophthalmol. 1999;14:95–108
9. 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
10. Broadway DC, Nicolela MT, Drance SM. Optic disk appearances in primary open-angle glaucoma. Surv Ophthalmol. 1999;43:S223–S243
11. 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
12. Burgoyne CF. A biomechanical paradigm for axonal insult within the optic nerve head in aging and glaucoma. Exp Eye Res. 2011;93:120–132
13. 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
14. 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
15. 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
16. Yoshikawa M, Akagi T, Hangai M, et al. Alterations in the neural and connective tissue components of glaucomatous cupping after glaucoma surgery using swept-source optical coherence tomography. Invest Ophthalmol Vis Sci. 2014;55:477–484
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. 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
19. 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
20. Albon J, Purslow PP, Karwatowski WS, Easty DL. Age related compliance of the lamina cribrosa in human eyes. Br J Ophthalmol. 2000;84:318–323
21. Albon J, Karwatowski WS, Avery N, Easty DL, Duance VC. Changes in the collagenous matrix of the aging human lamina cribrosa. Br J Ophthalmol. 1995;79:368–375
22. Albon J, Karwatowski WS, Easty DL, Sims TJ, Duance VC. Age related changes in the non-collagenous components of the extracellular matrix of the human lamina cribrosa. Br J Ophthalmol. 2000;84:311–317
23. Bailey AJ, Paul RG, Knott L. Mechanisms of maturation and ageing of collagen. Mech Ageing Dev. 1998;106:1–56
24. Kotecha A, Izadi S, Jeffrey G. Age related changes in the thickness of the human lamina cribrosa. Br J Ophthalmol. 2006;90:1531–1534
25. Fazio MA, Grytz R, Morris JS, et al. Age-related changes in human peripapillary scleral strain. Biomech Model Mechanobiol. 2014;13:551–563
26. 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
27. Coudrillier B, Tian J, Alexander S, Myers KM, Quigley HA, Nguyen TD. Biomechanics of the human posterior sclera: ageand glaucoma-related changes measured using inflation testing. Invest Ophthalmol Vis Sci. 2012;53:1714–1728
28. Rho CR, Park HY, Lee NY, Park CK. Clock-hour laminar displacement and age in primary open-angle glaucoma and normal tension glaucoma. Clin Experiment Ophthalmol. 2012;40:e183–e189
29. 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
30. Harwerth RS, Wheat JL, Rangaswamy NV. Age-related losses of retinal ganglion cells and axons. Invest Ophthalmol Vis Sci. 2008;49:4437–4443
31. Harwerth RS, Wheat JL, Fredette MJ, Anderson DR. Linking structure and function in glaucoma. Prog Retin Eye Res. 2010; 29:249–271
32. Burgoyne CF, Mercante DE, Thompson HW. Change detection in regional and volumetric disc parameters using longitudinal confocal scanning laser tomography. Ophthalmology. 2002; 109:455–466
33. Gardiner SK, Fortune B, Wang L, Downs JC, Burgoyne CF. Intraocular pressure magnitude and variability as predictors of rates of structural change in non-human primate experimental glaucoma. Exp Eye Res. 2012;103:1–8
34. Burgoyne CF, Quigley HA, Thompson HW, Vitale S, Varma R. Early changes in optic disc compliance and surface position in experimental glaucoma. Ophthalmology. 1995;102:1800–1809
35. Burgoyne CF, Quigley HA, Thompson HW, Vitale S, Varma R. Measurement of optic disc compliance by digitized image analysis in the normal monkey eye. Ophthalmology. 1995;102: 1790–1799
36. Chauhan BC, McCormick TA, Nicolela MT, LeBlanc RP. Optic disc and visual field changes in a prospective longitudinalstudy of patients with glaucoma: comparison of scanning laser tomography with conventional perimetry and optic disc photography. Arch Ophthalmol. 2001;119:1492–1499
37. Heickell AG, Bellezza AJ, Thompson HW, Burgoyne CF. Optic disc surface compliance testing using confocal scanning laser tomography in the normal monkey eye. J Glaucoma. 2001;10: 369–382
38. Fortune B, Reynaud J, Wang L, Burgoyne CF. Does optic nerve head surface topography change prior to loss of retinal nerve fiber layer thickness: a test of the site of injury hypothesis in experimental glaucoma. PLoS One. 2013;8:e77831
39. Chauhan BC, Blanchard JW, Hamilton DC, LeBlanc RP. Technique for detecting serial topographic changes in the optic disc and peripapillary retina using scanning laser tomography. Invest Ophthalmol Vis Sci. 2000;41:775–782
40. 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
41. Strouthidis NG, Grimm J, Williams GA, Cull GA, Wilson DJ, Burgoyne CF. A comparison of optic nerve head morphology viewed by spectral domain optical coherence tomography and by serial histology. Invest Ophthalmol Vis Sci. 2010;51:1464–1474
42. Yang H, Qi J, Hardin C, et al. Spectral-domain optical coherence tomography enhanced depth imaging of the normal and glaucomatous nonhuman primate optic nerve head. Invest Ophthalmol Vis Sci. 2012;53:394–405
43. 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
44. Qiao-Grider Y, Hung LF, Kee CS, Ramamirtham R, Smith EL III. A comparison of refractive development between two subspecies of infant rhesus monkeys (Macaca mulatta). Vision Res. 2007;47:1668–1681
45. Strouthidis NG, Fortune B, Yang H, Sigal IA, Burgoyne CF. Effect of acute intraocular pressure elevation on the monkey optic nerve head as detected by spectral domain optical coherence tomography. Invest Ophthalmol Vis Sci. 2011;52: 9431–9437
46. Medeiros FA, Lisboa R, Zangwill LM, et al. Evaluation of progressive neuroretinal rim loss as a surrogate end point for development of visual field loss in glaucoma. Ophthalmology. 2014;121:100–109
47. Chauhan BC, Nicolela MT, Artes PH. Incidence and rates of visual field progression after longitudinally measured optic disc change in glaucoma. Ophthalmology. 2009;116:2110–2118
48. Downs JC, Burgoyne CF, Seigfreid WP, Reynaud JF, Strouthidis NG, Sallee V. 24-hour IOP telemetry in the nonhuman primate: implant system performance and initial characterization of IOP at multiple timescales. Invest Ophthalmol Vis Sci. 2011;52: 7365–7375
49. 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.e2.