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August 1995, Vol 113, No. 8 >
ARTICLE | August 1995

Selective Loss of Blue Cones and Rods in Human Retinal Detachment FREE

T. Michael Nork, MD; Lyndell L. Millecchia, PhD; Bryan D. Strickland, MD; John V. Linberg, MD; Gung-mei Chao, PhD
Arch Ophthalmol. 1995;113(8):1066-1073. doi:10.1001/archopht.1995.01100080118039
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Comments

Objective:  To determine if there are histopathologic changes in the outer retina that could explain the blue-yellow color confusion previously described following rhegmatogenous retinal detachment in humans.

Methods:  Ten eyes with traumatic retinal detachments were studied. Eight of the eyes were removed from 2½ to 11 days following trauma. In the remaining two eyes, the retinas were successfully reattached. Enzyme histochemical studies for carbonic anhydrase and immunochemical studies for S antigen were performed to distinguish blue cones from red/green cones.

Results:  With the 2½- to 4-day-old detachments, nearly all of the carbonic anhydrase-negative (blue-sensitive) cones and many of the rods were seen to have signs of irreversible necrosis, including extreme swelling of the inner segments and mitochondria, loss of the outer segments, and pyknotic and displaced nuclei. In the 6- and 11-day-old detachments, almost all of the carbonic anhydrase-negative cones and many rods were missing. Blue cones were essentially absent from the reattached retinas, and there were only about half the normal number of rods.

Conclusions:  Rhegmatogenous retinal detachment results in rapid and almost total loss of the blue cones. Significant rod loss also occurs in this type of detachment but the red/green cones are comparatively resistant to damage. These findings could explain the observed blue-yellow color confusion in such patients. We discuss other clinical implications.

REFERENCES

1 +
Köllner H. Die Störungen des Farbensinnes, ihre klinische Bedeutung und ihre Diagnose . New York, NY: S Karger AG; 1912;:234-258.
2 +
Verriest G.  Further studies on acquired deficiency of color discrimination . J Opt Soc Am A . 1963;;53:185-195.
3 +
Marré M, Marré E.  Different types of acquired colour vision deficiencies on the base of CVM patterns in dependence upon the fixation mode of the diseased eye . Mod Probl Ophthalmol . 1978;;19:248-252.
4 +
Pokorny J, Smith VC, Verriest G, Pinckers AJLG, eds. Congenital and Acquired Color Vision Defects . New York, NY: Grune & Stratton; 1979;.
5 +
Koliopoulos J, Theodosiasdis G.  Retinal detachment and acquired colour vision disturbance . Mod Probl Ophthalmol . 1972;;11:117-121.
6 +
Drum B, Armaly MF, Huppert WE.  Sources of short wavelength sensitivity loss in glaucoma . Doc Ophthalmol . 1987;;46:413-422.
7 +
Gastaud P, Vola J, Saracco JB, de Galleani B, Costet C.  Diabetic dyschromatopsia: pathogenic hypothesis . Doc Ophthalmol . 1987;;46:387-390.
8 +
Marc RE, Sperling HG.  Chromatic organization of primate cones . Science . 1977;;196:454-456.
9 +
Sperling HG, Johnson C, Harwerth RS.  Differential spectral photic damage to primate cones . Vision Res . 1980;;20:1117-1125.
10 +
de Monasterio FM, Schein SJ, McCrane EP.  Staining of blue-sensitive cones of the macaque retina by a fluorescent dye . Science . 1981;;213:1278-1281.
11 +
McCrane EP, de Monasterio FM, Schein SJ, Caruso RC.  Non-fluorescent dye staining of primate blue cones . Invest Ophthalmol Vis Sci . 1983;;24:1449-1455.
12 +
de Monasterio FM, McCrane EP, Newlander JK, Schein SJ.  Density profile of blue-sensitive cones along the horizontal meridian of macaque retina . Invest Ophthalmol Vis Sci . 1985;;26:289-302.
13 +
Ahnelt PK, Kolb H, Pflug R.  Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina . J Comp Neurol . 1987;;255:18-34.
14 +
Szél Diamantstein T, Röhlich P.  Identification of the blue-sensitive cones in the mammalian retina by anti-visual pigment antibody . J Comp Neurol . 1988;;273:593-602.
15 +
Nork TM, McCormick SA, Chao GM, Odom JV.  Distribution of carbonic anhydrase among human photoreceptors . Invest Ophthalmol Vis Sci . 1990;;31:1451-1458.
16 +
Hood DC, Benimoff WI, Greenstein VC.  The response range of the blue-cone pathways: a source of vulnerability to disease . Invest Ophthalmol Vis Sci . 1984;;25:864-867.
17 +
Gündüz K, Arden GB, Perry S, Weinstein GW, Hitchings RA.  Color vision defects in ocular hypertension and glaucoma: quantification with a computerdriven color television system . Arch Ophthalmol . 1988;;106:929-935.
18 +
Mollon JD.  What is odd about the short-wavelength mechanism and why is it disproportionately vulnerable to acquired damage? report of a discussion . Doc Ophthalmol . 1983;;33:145-149.
19 +
Farnsworth D.  Tritanomalous vision as a threshold function . Farbe . 1955;;4:185-197.
20 +
Greenstein V, Hood DC, Campbell CJ.  The use of a flash-on-flash paradigm to assess sensitivity changes due to retinal disease . Invest Ophthalmol Vis Sci . 1982;;23:102-112.
21 +
Hart WMJ, Burde RM.  Three-dimensional topography of the central visual field: sparing of foveal sensitivity in macular disease . Ophthalmology . 1983;;90:1028-1038.
22 +
Hart WMJ.  Color contrast perimetry: hue discrimination defects in acquired dyschromatopsias . Doc Ophthalmol . 1987;;46:267-273.
23 +
Hart WMJ.  Acquired dyschromatopsias . Surv Ophthalmol . 1987;;32:10-31.
24 +
Nathans J, Thomas D, Hogness DS.  Molecular genetics of human color vision: the genes encoding blue, green and red pigments . Science . 1986;;232:193-202.
25 +
Nork TM, Mangini NJ, Millecchia LL.  Rods and cones contain antigenically distinctive S-antigens . Invest Ophthalmol Vis Sci . 1993;;34:2918-2925.
26 +
Köllner H.  Untersuchungen uber die Farbenstörung bei Netzhautablösung . Z Augenheilkd . 1907;;17:117-121.
27 +
Martin M, Menezo JC, Lopez H.  Alterations in colour vision in patients operated on for retinal detachment . Arch Soc Zsp Oftalmol . 1972;;32:793-808.
28 +
Chisholm A, McClure E, Foulds WS.  Functional recovery of the retina after retinal detachment . Eye . 1975;;95:167-172.
29 +
Marré M.  The investigation of acquired colour vision deficiencies . In: Hilger A, ed. Colour 73 . New York, NY: John Wiley & Sons Inc; 1973;:99-135.
30 +
Barca L, De Luca A, Passani F.  Color discrimination (100-hue test) after successful surgical treatment of retinal detachment . Doc Ophthalmol . 1985;;39:349-353.
31 +
Young RW.  The renewal of photoreceptor cell outer segments . J Cell Biol . 1967;;33:61-72.
32 +
Gundry MF, Davies EWG.  Recovery of visual acuity after retinal detachment surgery . Am J Ophthalmol . 1974;;77:310-314.
33 +
Grupposo SS.  Visual acuity following surgery for retinal detachment . Arch Ophthalmol . 1975;;93:327-330.
34 +
Burton TC.  Recovery of visual acuity after retinal detachment involving the macula . Trans Am Ophthalmol Soc . 1982;;80:475-497.
35 +
Kroll AJ, Machemer R.  Experimental retinal detachment in the owl monkey, Ill: electron microscopy of retina and pigment epithelium . Am J Ophthalmol . 1968;;66:410-427.
36 +
Anderson DH, Guerin CJ, Erickson PA, Stern WH, Fisher SK.  Morphological recovery in the reattached retina . Invest Ophthalmol Vis Sci . 1986;;27:168-183.
37 +
Guérin CJ, Anderson DH, Fariss RN, Fisher SK.  Retinal reattachment of the primate macula: photoreceptor recovery after short-term detachment . Invest Ophthalmol Vis Sci . 1989;;30:1708-1725.
38 +
Mangini NJ, Pepperberg DR.  Immunolocalization of 48K in rod photoreceptors: light and ATP increase OS labeling . Invest Ophthalmol Vis Sci . 1988;;29:1221-1234.
39 +
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.
40 +
Erickson PA, Fisher SK, Anderson DH, Stern WH, Borgula GA.  Retinal detachment in the cat: the outer nuclear and outer plexiform layers . Invest Ophthalmol Vis Sci . 1983;;24:927-942.
41 +
Wilson DJ, Green WR.  Histopathologic study of the effect of retinal detachment surgery on 49 eyes obtained post mortem . Am J Ophthalmol . 1987;;103:167-179.
42 +
Millecchia LL, Nork TM, Lemley H, Schochet T.  Regional damage to photoreceptors in humans eyes with chronic glaucoma . Invest Ophthalmol Vis Sci . 1992;;33( (suppl) ):1093.
43 +
Cook B, Lewis GP, Adler R, Fisher SK.  Photoreceptor degeneration in experimental retinal detachment: evidence for an apoptotic mechanism . Invest Ophthalmol Vis Sci . 1994;;35( (suppl) ):1833.
44 +
Osterberg GA.  Topology of the layer of rods and cones in the human retina . Acta Ophthalmol Suppl . 1935;;6:1-103.
45 +
Wald G.  Blue-blindness in the normal fovea . J Opt Soc Am A . 1967;;57:1289-1303.
46 +
Blight R, Hart JC.  Structural changes in the outer retinal layers following blunt mechanical non-perforating trauma to the globe: an experimental study . Br J Ophthalmol . 1977;;61:573-587.
47 +
Sipperley JO, Quigley HA, Gass DM.  Traumatic retinopathy in primates: the explanation of commotio retinae . Arch Ophthalmol . 1978;;96:2267-2273.
48 +
Bastek JV, Foos RY, Heckenlively J.  Traumatic pigmentary retinopathy . Am J Ophthalmol . 1981;;92:621-624.
49 +
Mansour AM, Green WR, Hogge C.  Histopathology of commotio retinae . Retina . 1992;;12:24-28.
50 +
Panda S, Jonas JB.  Decreased photoreceptor count in human eyes with secondary angle-closure glaucoma . Invest Ophthalmol Vis Sci . 1992;;33:2532-2536.
51 +
Nork TM, Poulsen GL, Vaegan, Sarks SH.  Photoreceptor damage and loss in human eyes with primary open angle glaucoma . Invest Ophthalmol Vis Sci . 1995;;36( (suppl) ):1546.
52 +
Ueda M, Adachi-Usami E.  Assessment of central visual function after successful retinal detachment surgery by pattern visual evoked cortical potentials . Br J Ophthalmol . 1992;;76:482-485.
53 +
Friberg TR, Eller AW.  Prediction of visual recovery after scleral buckling of macula-off retinal detachments . Am J Ophthalmol . 1992;;114:715-722.

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1 +
Köllner H. Die Störungen des Farbensinnes, ihre klinische Bedeutung und ihre Diagnose . New York, NY: S Karger AG; 1912;:234-258.
2 +
Verriest G.  Further studies on acquired deficiency of color discrimination . J Opt Soc Am A . 1963;;53:185-195.
3 +
Marré M, Marré E.  Different types of acquired colour vision deficiencies on the base of CVM patterns in dependence upon the fixation mode of the diseased eye . Mod Probl Ophthalmol . 1978;;19:248-252.
4 +
Pokorny J, Smith VC, Verriest G, Pinckers AJLG, eds. Congenital and Acquired Color Vision Defects . New York, NY: Grune & Stratton; 1979;.
5 +
Koliopoulos J, Theodosiasdis G.  Retinal detachment and acquired colour vision disturbance . Mod Probl Ophthalmol . 1972;;11:117-121.
6 +
Drum B, Armaly MF, Huppert WE.  Sources of short wavelength sensitivity loss in glaucoma . Doc Ophthalmol . 1987;;46:413-422.
7 +
Gastaud P, Vola J, Saracco JB, de Galleani B, Costet C.  Diabetic dyschromatopsia: pathogenic hypothesis . Doc Ophthalmol . 1987;;46:387-390.
8 +
Marc RE, Sperling HG.  Chromatic organization of primate cones . Science . 1977;;196:454-456.
9 +
Sperling HG, Johnson C, Harwerth RS.  Differential spectral photic damage to primate cones . Vision Res . 1980;;20:1117-1125.
10 +
de Monasterio FM, Schein SJ, McCrane EP.  Staining of blue-sensitive cones of the macaque retina by a fluorescent dye . Science . 1981;;213:1278-1281.
11 +
McCrane EP, de Monasterio FM, Schein SJ, Caruso RC.  Non-fluorescent dye staining of primate blue cones . Invest Ophthalmol Vis Sci . 1983;;24:1449-1455.
12 +
de Monasterio FM, McCrane EP, Newlander JK, Schein SJ.  Density profile of blue-sensitive cones along the horizontal meridian of macaque retina . Invest Ophthalmol Vis Sci . 1985;;26:289-302.
13 +
Ahnelt PK, Kolb H, Pflug R.  Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina . J Comp Neurol . 1987;;255:18-34.
14 +
Szél Diamantstein T, Röhlich P.  Identification of the blue-sensitive cones in the mammalian retina by anti-visual pigment antibody . J Comp Neurol . 1988;;273:593-602.
15 +
Nork TM, McCormick SA, Chao GM, Odom JV.  Distribution of carbonic anhydrase among human photoreceptors . Invest Ophthalmol Vis Sci . 1990;;31:1451-1458.
16 +
Hood DC, Benimoff WI, Greenstein VC.  The response range of the blue-cone pathways: a source of vulnerability to disease . Invest Ophthalmol Vis Sci . 1984;;25:864-867.
17 +
Gündüz K, Arden GB, Perry S, Weinstein GW, Hitchings RA.  Color vision defects in ocular hypertension and glaucoma: quantification with a computerdriven color television system . Arch Ophthalmol . 1988;;106:929-935.
18 +
Mollon JD.  What is odd about the short-wavelength mechanism and why is it disproportionately vulnerable to acquired damage? report of a discussion . Doc Ophthalmol . 1983;;33:145-149.
19 +
Farnsworth D.  Tritanomalous vision as a threshold function . Farbe . 1955;;4:185-197.
20 +
Greenstein V, Hood DC, Campbell CJ.  The use of a flash-on-flash paradigm to assess sensitivity changes due to retinal disease . Invest Ophthalmol Vis Sci . 1982;;23:102-112.
21 +
Hart WMJ, Burde RM.  Three-dimensional topography of the central visual field: sparing of foveal sensitivity in macular disease . Ophthalmology . 1983;;90:1028-1038.
22 +
Hart WMJ.  Color contrast perimetry: hue discrimination defects in acquired dyschromatopsias . Doc Ophthalmol . 1987;;46:267-273.
23 +
Hart WMJ.  Acquired dyschromatopsias . Surv Ophthalmol . 1987;;32:10-31.
24 +
Nathans J, Thomas D, Hogness DS.  Molecular genetics of human color vision: the genes encoding blue, green and red pigments . Science . 1986;;232:193-202.
25 +
Nork TM, Mangini NJ, Millecchia LL.  Rods and cones contain antigenically distinctive S-antigens . Invest Ophthalmol Vis Sci . 1993;;34:2918-2925.
26 +
Köllner H.  Untersuchungen uber die Farbenstörung bei Netzhautablösung . Z Augenheilkd . 1907;;17:117-121.
27 +
Martin M, Menezo JC, Lopez H.  Alterations in colour vision in patients operated on for retinal detachment . Arch Soc Zsp Oftalmol . 1972;;32:793-808.
28 +
Chisholm A, McClure E, Foulds WS.  Functional recovery of the retina after retinal detachment . Eye . 1975;;95:167-172.
29 +
Marré M.  The investigation of acquired colour vision deficiencies . In: Hilger A, ed. Colour 73 . New York, NY: John Wiley & Sons Inc; 1973;:99-135.
30 +
Barca L, De Luca A, Passani F.  Color discrimination (100-hue test) after successful surgical treatment of retinal detachment . Doc Ophthalmol . 1985;;39:349-353.
31 +
Young RW.  The renewal of photoreceptor cell outer segments . J Cell Biol . 1967;;33:61-72.
32 +
Gundry MF, Davies EWG.  Recovery of visual acuity after retinal detachment surgery . Am J Ophthalmol . 1974;;77:310-314.
33 +
Grupposo SS.  Visual acuity following surgery for retinal detachment . Arch Ophthalmol . 1975;;93:327-330.
34 +
Burton TC.  Recovery of visual acuity after retinal detachment involving the macula . Trans Am Ophthalmol Soc . 1982;;80:475-497.
35 +
Kroll AJ, Machemer R.  Experimental retinal detachment in the owl monkey, Ill: electron microscopy of retina and pigment epithelium . Am J Ophthalmol . 1968;;66:410-427.
36 +
Anderson DH, Guerin CJ, Erickson PA, Stern WH, Fisher SK.  Morphological recovery in the reattached retina . Invest Ophthalmol Vis Sci . 1986;;27:168-183.
37 +
Guérin CJ, Anderson DH, Fariss RN, Fisher SK.  Retinal reattachment of the primate macula: photoreceptor recovery after short-term detachment . Invest Ophthalmol Vis Sci . 1989;;30:1708-1725.
38 +
Mangini NJ, Pepperberg DR.  Immunolocalization of 48K in rod photoreceptors: light and ATP increase OS labeling . Invest Ophthalmol Vis Sci . 1988;;29:1221-1234.
39 +
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.
40 +
Erickson PA, Fisher SK, Anderson DH, Stern WH, Borgula GA.  Retinal detachment in the cat: the outer nuclear and outer plexiform layers . Invest Ophthalmol Vis Sci . 1983;;24:927-942.
41 +
Wilson DJ, Green WR.  Histopathologic study of the effect of retinal detachment surgery on 49 eyes obtained post mortem . Am J Ophthalmol . 1987;;103:167-179.
42 +
Millecchia LL, Nork TM, Lemley H, Schochet T.  Regional damage to photoreceptors in humans eyes with chronic glaucoma . Invest Ophthalmol Vis Sci . 1992;;33( (suppl) ):1093.
43 +
Cook B, Lewis GP, Adler R, Fisher SK.  Photoreceptor degeneration in experimental retinal detachment: evidence for an apoptotic mechanism . Invest Ophthalmol Vis Sci . 1994;;35( (suppl) ):1833.
44 +
Osterberg GA.  Topology of the layer of rods and cones in the human retina . Acta Ophthalmol Suppl . 1935;;6:1-103.
45 +
Wald G.  Blue-blindness in the normal fovea . J Opt Soc Am A . 1967;;57:1289-1303.
46 +
Blight R, Hart JC.  Structural changes in the outer retinal layers following blunt mechanical non-perforating trauma to the globe: an experimental study . Br J Ophthalmol . 1977;;61:573-587.
47 +
Sipperley JO, Quigley HA, Gass DM.  Traumatic retinopathy in primates: the explanation of commotio retinae . Arch Ophthalmol . 1978;;96:2267-2273.
48 +
Bastek JV, Foos RY, Heckenlively J.  Traumatic pigmentary retinopathy . Am J Ophthalmol . 1981;;92:621-624.
49 +
Mansour AM, Green WR, Hogge C.  Histopathology of commotio retinae . Retina . 1992;;12:24-28.
50 +
Panda S, Jonas JB.  Decreased photoreceptor count in human eyes with secondary angle-closure glaucoma . Invest Ophthalmol Vis Sci . 1992;;33:2532-2536.
51 +
Nork TM, Poulsen GL, Vaegan, Sarks SH.  Photoreceptor damage and loss in human eyes with primary open angle glaucoma . Invest Ophthalmol Vis Sci . 1995;;36( (suppl) ):1546.
52 +
Ueda M, Adachi-Usami E.  Assessment of central visual function after successful retinal detachment surgery by pattern visual evoked cortical potentials . Br J Ophthalmol . 1992;;76:482-485.
53 +
Friberg TR, Eller AW.  Prediction of visual recovery after scleral buckling of macula-off retinal detachments . Am J Ophthalmol . 1992;;114:715-722.

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