Human chorioretinal layer thicknesses measured in macula-wide, high-resolution histologic sections

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 7, 2011, Pages 3943-3954

  Curcio, Christine A ^a   Messinger, Jeffrey D ^a   Sloan, Kenneth R ^a   Mitra, Arnab ^a   McGwin, Gerald ^a   Spaide, Richard F ^b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b VITREOUS RETINA MACULA CONSULTANTS OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGE DISTRIBUTION; AGED; ARTICLE; CHORIORETINAL LAYER THICKNESS; CONTROLLED STUDY; EX VIVO STUDY; HUMAN; HUMAN TISSUE; PRIORITY JOURNAL; RETINA DETACHMENT; RETINA GANGLION CELL; RETINA INNER PLEXIFORM LAYER; RETINA MACULA LUTEA; SIGNAL TRANSDUCTION; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; TISSUE DISTRIBUTION; TISSUE SECTION; VALIDATION PROCESS; VISUAL SYSTEM PARAMETERS;

ADULT; AGED; AGED, 80 AND OVER; CHOROID; DATABASES, FACTUAL; EYE BANKS; FEMALE; HUMANS; MACULA LUTEA; MALE; MICROTOMY; MIDDLE AGED; NEUROANATOMY; REFERENCE VALUES; RETINAL GANGLION CELLS; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 79958185131     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-6377     Document Type: Article

References (99)

1. Polyak SL. The Retina. Chicago: University of Chicago; 1941.
2. Klein R, Davis MD, Magli YL, Segal P, Klein BEK, Hubbard L. The Wisconsin Age-Related Maculopathy Grading System. Ophthalmology. 1991;98:1128-1134.
3. Boycott BB, Dowling JE. Organization of the primate retina: light microscopy. Phil Trans Roy Soc Lond B. 1969;255:109-184.
4. Hogan MJ, Alvarado JA, Weddell JE. Histology of the human eye. An Atlas and Textbook. Philadelphia: WB Saunders; 1971.
5. Schein SJ. Anatomy of macaque fovea and spatial densities of neurons in foveal representation. J Comp Neurol. 1988;269:479-505.
6. Ahnelt PK, Pflug R. Telodendrial contacts between foveolar cone pedicles in the human retina. Experientia. 1986;42:298-300.
7. Bressler SB, Bressler NM, Sarks SH, Sarks JP. Age-related macular degeneration: nonneovascular early AMD, intermediate AMD, and geographic atrophy. In: Ryan SJ, ed. Retina. St. Louis: Mosby;2006: 1041-1074.
8. Sarks S, Cherepanoff S, Killingsworth M, Sarks J. Relationship of basal laminar deposit and membranous debris to the clinical presentation of early age-related macular degeneration. Invest Ophthalmol Vis Sci. 2007;48:968-977.
9. Rudolf M, Malek G, Messinger JD, Wang L, Clark ME, Curcio CA. Sub-retinal drusenoid deposits in human retina: organization and composition. Exp Eye Res. 2008;87:402-408.
10. Elman MJ, Aiello LP, Beck RW, et al. Randomized trial evaluating ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Ophthalmology. 2010; 117:1064-1077, e35.
11. Diabetic Retinopathy Clinical Research Network. A randomized trial comparing intravitreal triamcinolone acetonide and focal/grid photocoagulation for diabetic macular edema. Ophthalmology. 2008;115:1447-1449, e1-e10.
12. Nguyen QD, Shah SM, Heier JS, et al. Primary end point (six months) results of the ranibizumab for edema of the macula in diabetes (READ-2) study. Ophthalmology. 2009;116:2175-2181, e1.
13. Spaide RF, Chang LK, Klancnik JM, et al. Prospective study of intravitreal ranibizumab as a treatment for decreased visual acuity secondary to central retinal vein occlusion. Am J Ophthalmol. 2009;147:298-306.
14. Campochiaro PA, Heier JS, Feiner L, et al. Ranibizumab for macular edema following branch retinal vein occlusion: six-month primary end point results of a phase III study. Ophthalmology. 2010;117: 1102-1112, e1.
15. Khanifar AA, Koreishi AF, Izatt JA, Toth CA. Drusen ultrastructure imaging with spectral domain optical coherence tomography in age-related macular degeneration. Ophthalmology. 2008;115: 1883-1890.
16. Drexler W, Sattmann H, Hermann B, et al. Enhanced visualization of macular pathology with the use of ultrahigh-resolution optical coherence tomography. Arch Ophthalmol. 2003;121: 695-706.
17. Wolf-Schnurrbusch UE, Enzmann V, Brinkmann CK, Wolf S. Morphologic changes in patients with geographic atrophy assessed with a novel spectral OCT-SLO combination. Invest Ophthalmol Vis Sci. 2008;49:3095-3099.
18. Yi K, Mujat M, Park BH, et al. Spectral domain optical coherence tomography for quantitative evaluation of drusen and associated structural changes in non-neovascular age-related macular degeneration. Br J Ophthalmol. 2009;93:176-181.
19. Unterhuber A, Povazäy B, Hermann B, Sattmann H, Chavez-Pirson A, Drexler W. In vivo retinal optical coherence tomography at 1040 nm: enhanced penetration into the choroid. Opt Express. 2005;13:3252-3258.
20. Spaide RF, Koizumi H, Pozonni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol. 2008;146:496-500.
21. Toth CA, Narayan DG, Boppart SA, et al. A comparison of retinal morphology viewed by optical coherence tomography and by light microscopy. Arch Ophthalmol. 1997;115:1425-1428.
22. Yabushita H, Bouma BE, Houser SL, et al. Characterization of human atherosclerosis by optical coherence tomography. Circulation. 2002;106:1640-1645.
23. Cilingiroglu M, Oh JH, Sugunan B, et al. Detection of vulnerable plaque in a murine model of atherosclerosis with optical coherence tomography. Catheter Cardiovasc Interv. 2006;67:915-923.
24. Gambichler T, Moussa G, Regeniter P, et al. Validation of optical coherence tomography in vivo using cryostat histology. Phys Med Biol. 2007;52:N75-N85.
25. Drexler W, Fujimoto JG. State-of-the-art retinal optical coherence tomography. Prog Retin Eye Res. 2008;27:45-88.
26. Drexler W, Morgner U, Ghanta RK, Kartner FX, Schuman JS, Fujimoto JG. Ultrahigh-resolution ophthalmic optical coherence tomography. Nat Med. 2001;7:502-507.
27. Costa RA, Calucci D, Skaf M, et al. Optical coherence tomography 3: automatic delineation of the outer neural retinal boundary and its influence on retinal thickness measurements. Invest Ophthalmol Vis Sci. 2004;45:2399-2406.
28. Ko TH, Fujimoto JG, Duker JS, et al. Comparison of ultrahigh-and standard-resolution optical coherence tomography for imaging macular hole pathology and repair. Ophthalmology. 2004;111: 2033-2043.
29. Hangai M, Yamamoto M, Sakamoto A, Yoshimura N. Ultrahighresolution versus speckle noise-reduction in spectral-domain optical coherence tomography. Opt Express. 2009;17:4221-4235.
30. Tanna H, Dubis AM, Ayub N, et al. Retinal imaging using commercial broadband optical coherence tomography. Br J Ophthalmol. 2010;94:372-376.
31. Anger EM, Unterhuber A, Hermann B, et al. Ultrahigh resolution optical coherence tomography of the monkey fovea: identification of retinal sublayers by correlation with semithin histology sections. Exp Eye Res. 2004;78:1117-1125.
32. Zawadzki RJ, Jones SM, Olivier SS, et al. Adaptive-optics optical coherence tomography for high-resolution and high-speed 3D retinal in vivo imaging. Opt Express. 2005;13:8532-8546.
33. Coscas G, Coscas F, Vismara S, Souied E, Soubrane G. Spectral domain OCT in age-related macular degeneration: preliminary results with Spectralis HRA-OCT (in French). J Fr Ophtalmol. 2008; 31:353-361.
34. Fernández EJ, Hermann B, Povazay B, et al. Ultrahigh resolution optical coherence tomography and pancorrection for cellular imaging of the living human retina. Opt Express. 2008;16:11083-11094.
35. Cucu RG, Podoleanu AG, Rogers JA, Pedro J, Rosen RB. Combined confocal/en face T-scan-based ultrahigh-resolution optical coherence tomography in vivo retinal imaging. Opt Lett. 2006;31:1684-1686.
36. Michels S, Pircher M, Geitzenauer W, et al. Value of polarisationsensitive optical coherence tomography in diseases affecting the retinal pigment epithelium. Br J Ophthalmol. 2008;92:204-209.
37. Srinivasan VJ, Monson BK, Wojtkowski M, et al. Characterization of outer retinal morphology with high-speed, ultrahigh-resolution optical coherence tomography. Invest Ophthalmol Vis Sci. 2008; 49:1571-1579.
38. Huang Y, Cideciyan AV, Papastergiou GI, et al. Relation of optical coherence tomography to microanatomy in normal and rd chickens. Invest Ophthalmol Vis Sci. 1998;39:2405-2416.
39. Fischer MD, Huber G, Beck SC, et al. Noninvasive, in vivo assessment of mouse retinal structure using optical coherence tomography. PLoS One. 2009;4:e7507.
40. Srinivasan VJ, Ko TH, Wojtkowski M, et al. Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography. Invest Ophthalmol Vis Sci. 2006;47:5522-5528.
41. Gloesmann M, Hermann B, Schubert C, Sattmann H, Ahnelt PK, Drexler W. Histologic correlation of pig retina radial stratification with ultrahigh-resolution optical coherence tomography. Invest Ophthalmol Vis Sci. 2003;44:1696-1703.
42. Abbott CJ, McBrien NA, Grunert U, Pianta MJ. Relationship of the optical coherence tomography signal to underlying retinal histology in the tree shrew (Tupaia belangeri). Invest Ophthalmol Vis Sci. 2009;50:414-423.
43. Chauhan DS, Marshall J. The interpretation of optical coherence tomography images of the retina. Invest Ophthalmol Vis Sci. 1999;40:2332-2342.
44. Chen TC, Cense B, Miller JW, et al. Histologic correlation of in vivo optical coherence tomography images of the human retina. Am J Ophthalmol. 2006;141:1165-1168.
45. Ghazi NG, Dibernardo C, Ying HS, Mori K, Gehlbach PL. Optical coherence tomography of enucleated human eye specimens with histological correlation: origin of the outer "red line. " Am J Ophthalmol. 2006;141:719-726.
46. Brown NH, Koreishi AF, McCall M, Izatt JA, Rickman CB, Toth CA. Developing SDOCT to assess donor human eyes prior to tissue sectioning for research. Graefes Arch Clin Exp Ophthalmol. 2009; 247:1069-1080.
47. Guyton JR, Klemp KF. Ultrastructural discrimination of lipid droplets and vesicles in atherosclerosis: value of osmium-thiocarbohydrazide-osmium and tannic acid-paraphenylenediamine techniques. J Histochem Cytochem. 1988;36:1319-1328.
48. Curcio CA, Millican CL, Bailey T, Kruth HS. Accumulation of cholesterol with age in human Bruch's membrane. Invest Ophthalmol Vis Sci. 2001;42:265-274.
49. Bagci AM, Shahidi M, Ansari R, Blair M, Blair NP, Zelkha R. Thickness profiles of retinal layers by optical coherence tomography image segmentation. Am J Ophthalmol. 2008;146:679-687.
50. Drasdo N, Millican CL, Katholi CR, Curcio CA. The length of Henle fibers in the human retina and a model of ganglion receptive field density in the visual field. Vision Res. 2007;47:2901-2911.
51. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1986;1: 307-310.
52. Wojtkowski M, Srinivasan V, Ko T, Fujimoto J, Kowalczyk A, Duker J. Ultrahigh-resolution, high-speed, Fourier domain optical coherence tomography and methods for dispersion compensation. Opt Express. 2004;12:2404-2422.
53. Fleckenstein M, Charbel Issa P, Helb HM, et al. High-resolution spectral domain-OCT imaging in geographic atrophy associated with age-related macular degeneration. Invest Ophthalmol Vis Sci. 2008;49:4137-4144.
54. Falkenberry SM, Ip MS, Blodi BA, Gunther JB. Optical coherence tomography findings in central retinal artery occlusion. Ophthalmic Surg Lasers Imaging. 2006;37:502-505.
55. Margolis R, Spaide RF. A pilot study of enhanced depth imaging optical coherence tomography of the choroid in normal eyes. Am J Ophthalmol. 2009;147:811-815.
56. Curcio CA, Sloan KR, Kalina RE, Hendrickson AE. Human photoreceptor topography. J Comp Neurol. 1990;292:497-523.
57. Sarks JP, Sarks SH, Killingsworth MC. Evolution of geographic atrophy of the retinal pigment epithelium. Eye. 1988;2:552-577.
58. Curcio CA, Presley JB, Millican CL, Medeiros NE. Basal deposits and drusen in eyes with age-related maculopathy: evidence for solid lipid particles. Exp Eye Res. 2005;80:761-775.
59. Curcio CA, Millican CL. Basal linear deposit and large drusen are specific for early age-related maculopathy. Arch Ophthalmol. 1999;117:329-339.
60. Sarks SH. Ageing and degeneration in the macular region: a clinicopathological study. Br J Ophthalmol. 1976;60:324-341. PMID 952802.
61. van der Schaft TL, Mooy CM, de Bruijn WC, Oron FG, Mulder PGH, de Jong PTVM. Histologic features of the early stages of age-related macular degeneration. Ophthalmol. 1992;99:278-286.
62. Spraul CW, Grossniklaus HE. Characteristics of drusen and Bruch's membrane in postmortem eyes with age-related macular degeneration. Arch Ophthalmol. 1997;115:267-273.
63. Malek G, Li C-M, Guidry C, Medeiros NE, Curcio CA. Apolipoprotein B in cholesterol-containing drusen and basal deposits in eyes with age-related maculopathy. Am J Pathol. 2003;162:413-425.
64. Huang Y, Cideciyan AV, Aleman TS, et al. Optical coherence tomography (OCT) abnormalities in rhodopsin mutant transgenic swine with retinal degeneration. Exp Eye Res. 2000;70:247-251.
65. Giani A, Cigada M, Choudhry N, et al. Reproducibility of retinal thickness measurements on normal and pathologic eyes by different optical coherence tomography instruments. Am J Ophthalmol. 2010;150:815-824.
66. Grover S, Murthy RK, Brar VS, Chalam KV. Comparison of retinal thickness in normal eyes using Stratus and Spectralis optical coherence tomography. Invest Ophthalmol Vis Sci. 2010;51:2644-2647.
67. Hendrickson A. Organization of the human fovea. In: Penfold PL, Provis JM, eds. Macular Degeneration. Berlin: Springer-Verlag; 2005:1-24.
68. Curcio CA, Allen KA. Topography of ganglion cells in human retina. J Comp Neurol. 1990;300:5-25.
69. Wässle H, Grünert U, Rohrenbeck J, Boycott BB. Cortical magnification factor and the retinal ganglion cell density in the primate. Nature. 1989;341:643-646.
70. Hsu A, Tsukamoto Y, Smith RG, Sterling P. Functional architecture of primate cone and rod axons. Vision Res. 1998;38:2539-2549.
71. Wassle H. Parallel processing in the mammalian retina. Nat Rev Neurosci. 2004;5:747-757.
72. Pircher M, Gotzinger E, Leitgeb R, Sattmann H, Findl O, Hitzenberger C. Imaging of polarization properties of human retina in vivo with phase resolved transversal PS-OCT. Opt Express. 2004; 12:5940-5951.
73. Pircher M, Gotzinger E, Findl O, et al. Human macula investigated in vivo with polarization-sensitive optical coherence tomography. Invest Ophthalmol Vis Sci. 2006;47:5487-5494.
74. Lujan B, Roorda A, Knighton RW, Carroll J. Revealing Henle's fiber layer using spectral domain optical coherence tomography. Invest Ophthalmol Vis Sci. 2011;52:1486-1492.
75. Otani T, Yamaguchi Y, Kishi S. Improved visualization of Henle fiber layer by changing the measurement beam angle on optical coherence tomography. Retina. 2010.
76. Spaide RF. Age-related choroidal atrophy. Am J Ophthalmol. 2009; 147:801-810.
77. Ramrattan RS, van der Schaft TL, Mooy CM, de Bruijn WC, Mulder PGH, de Jong PTVM. Morphometric analysis of Bruch's membrane, the choriocapillaris, and the choroid in aging. Invest Ophthalmol Vis Sci. 1994;35:2857-2864.
78. Thumann G, Hoffman S, Hinton DR. Cell biology of the retinal pigment epithelium. In: Ryan SJ, ed. Retina. St. Louis: Mosby; 2006:1041-1074.
79. Feeney-Burns L, Burns RP, Gao C-L. Age-related macular changes in humans over 90 years old. Am J Ophthalmol. 1990;109:265-278.
80. Gao H, Hollyfield JG. Aging of the human retina. Differential loss of neurons and retinal pigment epithelial cells. Invest Ophthalmol Vis Sci. 1992;33:1-17.
81. Del Priore LV, Kuo Y-H, Tezel TH. Age-related changes in human RPE cell density and apoptosis proportion in situ. Invest Ophthalmol Vis Sci. 2002;43:3312-3318.
82. Harman AM, Fleming PA, Hoskins RV, Moore SR. Development and aging of cell topography in the human retinal pigment epithelium. Invest Ophthalmol Vis Sci. 1997;38:2016-2026.
83. Panda-Jonas S, Jonas JB, Jakobczyk-Zmija M. Retinal pigment epithelial cell count, distribution, and correlations in normal human eyes. Am J Ophthalmol. 1996;121:181-189.
84. Morgan JI, Dubra A, Wolfe R, Merigan WH, Williams DR. In vivo autofluorescence imaging of the human and macaque retinal pigment epithelial cell mosaic. Invest Ophthalmol Vis Sci. 2009;50: 1350-1359.
85. Grunwald JE, Hariprasad SM, DuPont J. Effect of aging on foveolar choroidal circulation. Arch Ophthalmol. 1998;116:150-154.
86. Fitzgerald ME, Tolley E, Frase S, et al. Functional and morphological assessment of age-related changes in the choroid and outer retina in pigeons. Vis Neurosci. 2001;18:299-317.
87. Curcio CA, Millican CL, Allen KA, Kalina RE. Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina. Invest Ophthalmol Vis Sci. 1993;34: 3278-3296.
88. Bringmann A, Pannicke T, Grosche J, et al. Muller cells in the healthy and diseased retina. Prog Retin Eye Res. 2006;25:397-424.
89. DiLoreto DA Jr, Martzen MR, del Cerro C, Coleman PD, del Cerro M. Muller cell changes precede photoreceptor cell degeneration in the age-related retinal degeneration of the Fischer 344 rat. Brain Res. 1995;698:1-14.
90. Madigan MC, Penfold PL, Provis JM, Balind TK, Billson FA. Intermediate filament expression in human retinal macroglia: histo-pathologic changes associated with age-related macular degeneration. Retina. 1994;14:65-74.
91. Wu KH, Madigan MC, Billson FA, Penfold PL. Differential expression of GFAP in early v late AMD: a quantitative analysis. Br J Ophthalmol. 2003;87:1159-1166.
92. Grosche J, Grimm D, Clemens N, Reichenbach A. Retinal light damage vs. normal aging of rats: altered morphology, intermediate filament expression, and nuclear organization of Muller (glial) cells. J Hirnforsch. 1997;38:459-470.
93. Harwerth RS, Wheat JL. Modeling the effects of aging on retinal ganglion cell density and nerve fiber layer thickness. Graefes Arch Clin Exp Ophthalmol. 2008;246:305-314.
94. Harwerth RS, Wheat JL, Rangaswamy NV. Age-related losses of retinal ganglion cells and axons. Invest Ophthalmol Vis Sci. 2008; 49:4437-4443.
95. Guidry C, Medeiros NE, Curcio CA. Phenotypic variation of retinal pigment epithelium in age-related macular degeneration. Invest Ophthalmol Vis Sci. 2002;43:267-273.
96. Fujiwara T, Imamura Y, Margolis R, Slakter JS, Spaide RF. Enhanced depth imaging optical coherence tomography of the choroid in highly myopic eyes. Am J Ophthalmol. 2009;148: 445-450.
97. Budenz DL, Anderson DR, Varma R, et al. Determinants of normal retinal nerve fiber layer thickness measured by Stratus OCT. Ophthalmology. 2007;114:1046-1052.
98. Alamouti B, Funk J. Retinal thickness decreases with age: an OCT study. Br J Ophthalmol. 2003;87:899-901.
99. Neuville JM, Bronson-Castain K, Bearse MA Jr, et al. OCT reveals regional differences in macular thickness with age. Optom Vis Sci. 2009;86:E810-E816.