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January 1994, Vol 112, No. 1 >
ARTICLE | January 1994

Localization and Quantitation of Blood-Retinal Barrier Breakdown in Experimental Proliferative Vitreoretinopathy FREE

Noburo Ando, MD; Harsha A. Sen, MD; Bruce A. Berkowitz, PhD; Charles A. Wilson, MD; Eugene de Juan, Jr, MD
Arch Ophthalmol. 1994;112(1):117-122. doi:10.1001/archopht.1994.01090130127029
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Objective:  To determine the contribution of the break-down of the blood-retinal barrier (BRB) as measured with magnetic resonance imaging in the development of retinal detachment in an experimental model of proliferative vitreoretinopathy.

Methods:  Contrast-enhanced magnetic resonance imaging was used to evaluate BRB breakdown in an intravitreal cell-injection model of proliferative vitreoretinopathy. Intravitreal injection of 2.5×105 homologous dermal fibroblasts produced specific disruption of the inner, or vascular, BRB.

Results:  Breakdown of the BRB was greatest in the first 3 days after injection, confirming previous work using fluorescein-based methods. Injection of 1 mg of intravitreal triamcinolone acetonide at the time of cell injection significantly reduced both BRB breakdown and the incidence of eventual traction retinal detachment. Eyes that did develop detachment had significantly greater leakage prior to its development than those that did not, regardless of steroid treatment.

Conclusions:  Quantitation and definitive localization of BRB leakage with magnetic resonance imaging provides a better understanding of the relationship between BRB compromise and the development of retinal detachment in this frequently used model.

REFERENCES

1 +
Kampik A, Kenyon KR, Michels RG, et al.  Epiretinal and vitreous membranes: a comparative study of 56 cases . Arch Ophthalmol . 1981;;99:1445-1454.
2 +
Laqua H, Machemer R.  Clinical-pathologic correlation in massive periretinal proliferation . Am J Ophthalmol . 1975;;80:913-929.
3 +
Machemer R.  Massive periretinal proliferation: a logical approach to therapy . Trans Am Ophthalmol Soc . 1977;;75:556-586.
4 +
Sternberg P, Machemer R.  Result of conventional vitreous surgery for vitreoretinopathy . Am J Ophthalmol . 1985;;100:141-146.
5 +
Sunalp M, Wiedemann D, Sorgente NJ, Ryan T.  Effects of cytotoxic drugs on proliferative vetreoretinopathy in the rabbit cell injection model . Curr Eye Res . 1984;;34:619-623.
6 +
Sen HA, Robertson TJ, Conway BP, Campochiaro PA.  The role of breakdown of the blood-retinal barrier in cell-injection models of proliferative vitreoretinopathy . Arch Ophthalmol . 1988;;106:1291-1294.
7 +
Campochiaro PA, Sen HA, Robertson TJ, Conway BP.  The role of breakdown of the blood-retinal barrier in proliferative vitreoretinopathy . In: Proliferative Vitreoretinopathy . Heidelberg, Germany: Kadon Verlag; 1989;;45-49.
8 +
The Retina Society Terminology Committee.  Classification of retinal detachment with proliferative vitreoretinopathy . Ophthalmology . 1983;;90:121-125.
9 +
Campochiaro PA, Bryan JA III, Conway BP, Jaccoma EH.  Intravitreal chemotactic and mitogenic activity: implication of blood-retinal barrier breakdown . Arch Ophthalmol . 1986;;104:1685-1687.
10 +
Algvere PV, Hallnas K, Dafgard E, Hoog A.  Panretinal photocoagulation aggravates experimental proliferative vitreoretinopathy . Graefes Arch Clin Exp Ophthalmol . 1990;;228:461-466.
11 +
Campochiaro PA, Gaskin HC, Vinores SA.  Retinal cryopexy stimulates traction retinal detachment formation in the presence of an ocular wound . Arch Ophthalmol . 1987;;105:1567-1570.
12 +
Campochiaro PA, Jerdan JA, Glaser BM.  Serum contains chemoattractants for human retinal pigment epithelial cells . Arch Ophthalmol . 1984;;102:1830-1833.
13 +
Campochiaro PA, Glaser BM.  Platelet-derived growth factor is chemotactic for human retinal pigment epithelial cells . Arch Ophthalmol . 1985;;103:576-579.
14 +
Gauss-Muller V, Kleinman H, Martin GR, et al.  Role of attachment and attractants in fibroblast chemotaxis . J Lab Clin Med . 1980;;96:1071-1080.
15 +
de Juan E Jr, Dickson J, Hjelmeland L.  Serum is chemotactic for retinal-derived glial cells . Arch Ophthalmol . 1988;;106:986-990.
16 +
Cunha-Vaz JG.  The blood-ocular barriers . Surv Ophthalmol . 1979;;23:279-296.
17 +
Bito LZ, DeRousseau CJ.  Transport functions of the blood-retinal barrier system and the microenvironment of the retina . In: Cunha-Vaz JG, ed. The Blood-Retinal Barriers . New York, NY: Plenum Press; 1980;:133-163.
18 +
Conway BP.  Technical variables in vitreous fluorophotometry . Graefes Arch Clin Exp Ophthalmol . 1985;;222:194-201.
19 +
Plehwe WE, McRobbie DW, Lerski RA, Kohner EM.  Quantitative MRI in assessment of the blood-retinal barrier . Invest Ophthalmol Vis Sci . 1988;;29:663-670.
20 +
Berkowitz BA, Sato Y, Wilson DA, de Juan E Jr.  Blood retinal barrier breakdown investigated by real-time MRI following Gd-DTPA injection . Invest Ophthalmol Vis Sci . 1991;;32:2854-2860.
21 +
Sato Y, Berkowitz BA, Wilson CA, de Juan E Jr.  Blood-retinal barrier break-down caused by diode and argon laser endophotocoagulation: a comparative MRI study . Arch Ophthalmol . 1992;;110:277-281.
22 +
Berkowitz BA, Tofts P, Sen HA, Ando N, de Juan E Jr.  Accurate and precise measurement of blood-retinal barrier breakdown using dynamic Gd-DTPA MRI . Invest Ophthalmol Vis Sci . 1992;;33:3500-3506.
23 +
Sen HA, Berkowitz BA, Ando N, de Juan E Jr.  In vivo imaging of breakdown of the inner and outer blood-retinal barriers . Invest Ophthalmol Vis Sci . 1992;;33:3507-3512.
24 +
Sugita G, Tano Y, Machemer R, et al.  Intravitreal autotransplantation of fibroblasts . Am J Ophthalmol . 1980;;89:121-130.
25 +
Chandler DB, Hida T, Sheta S, et al.  Improvement in efficacy of corticosteroid therapy in an animal model of proliferative vitreoretinopathy by pretreatment . Graefes Arch Clin Exp Ophthalmol . 1987;;225:259-265.
26 +
Tano Y, Chandler D, Machemer R.  Treatment of intraocular proliferation with intravitreal injection of triamcinolone acetonide . Am J Ophthalmol . 1980;;90:810-816.
27 +
Wyatt JD, Scott RAW, Richardson ME.  The effect of prolonged ketamine-xylazine intravenous infusion on arterial blood pH, blood gases, mean arterial blood pressure, heart and respiratory rates, rectal temperature and reflexes in the rabbit . Lab Anim Sci . 1989;;39:411-416.
28 +
de Juan E Jr, Humayun M, Wilson D, Hatchell D.  Histopathology of experimental preretinal neovascularization . Invest Ophthalmol Vis Sci . 1989;;30:1495-1503.
29 +
de Juan E Jr, Wilson D, Hatchell D.  Breakdown of the blood-retinal barrier in a model of retinal neovascularization . Invest Ophthalmol Vis Sci . 1987;;28:1108-1115.
30 +
Hatchell DL, McAdoo T, Sheta S, et al.  Quantification of cellular proliferation in experimental proliferative vitreoretinopathy . Arch Ophthalmol . 1988;;106:669-672.
31 +
Fastenberg DM, Diddie KR, Dorey K, Ryan SJ.  The role of cellular proliferation in an experimental model of massive periretinal proliferation . Am J Ophthalmol . 1982;;93:565-572.
32 +
Tano Y, Sugita G, Abrams G, Machemer R.  Inhibition of intraocular proliferations with intravitreal corticosteroids . Am J Ophthalmol . 1980;;89:131-136.
33 +
McCuen BW, Bessler M, Tano Y, et al.  The lack of toxicity of intravitreally administered triamcinolone acetonide . Am J Ophthalmol . 1981;;91:785-788.
34 +
Ruhmann AG, Berliner DL.  Effect of steroids on growth of mouse fibroblasts in vitro . Endocrinology . 1965;;76:916-920.
35 +
Dannenberg AM.  The anti-inflammatory effects of glucocorticosteroids: a brief review of the literature . Inflammation . 1979;;3:329-343.
36 +
Blankenship GW.  Evaluation of a single intravitreal injection of dexamethasone phosphate in vitrectomy surgery for diabetic retinopathy complications . Graefes Arch Clin Exp Ophthalmol . 1991;;229:62-65.

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1 +
Kampik A, Kenyon KR, Michels RG, et al.  Epiretinal and vitreous membranes: a comparative study of 56 cases . Arch Ophthalmol . 1981;;99:1445-1454.
2 +
Laqua H, Machemer R.  Clinical-pathologic correlation in massive periretinal proliferation . Am J Ophthalmol . 1975;;80:913-929.
3 +
Machemer R.  Massive periretinal proliferation: a logical approach to therapy . Trans Am Ophthalmol Soc . 1977;;75:556-586.
4 +
Sternberg P, Machemer R.  Result of conventional vitreous surgery for vitreoretinopathy . Am J Ophthalmol . 1985;;100:141-146.
5 +
Sunalp M, Wiedemann D, Sorgente NJ, Ryan T.  Effects of cytotoxic drugs on proliferative vetreoretinopathy in the rabbit cell injection model . Curr Eye Res . 1984;;34:619-623.
6 +
Sen HA, Robertson TJ, Conway BP, Campochiaro PA.  The role of breakdown of the blood-retinal barrier in cell-injection models of proliferative vitreoretinopathy . Arch Ophthalmol . 1988;;106:1291-1294.
7 +
Campochiaro PA, Sen HA, Robertson TJ, Conway BP.  The role of breakdown of the blood-retinal barrier in proliferative vitreoretinopathy . In: Proliferative Vitreoretinopathy . Heidelberg, Germany: Kadon Verlag; 1989;;45-49.
8 +
The Retina Society Terminology Committee.  Classification of retinal detachment with proliferative vitreoretinopathy . Ophthalmology . 1983;;90:121-125.
9 +
Campochiaro PA, Bryan JA III, Conway BP, Jaccoma EH.  Intravitreal chemotactic and mitogenic activity: implication of blood-retinal barrier breakdown . Arch Ophthalmol . 1986;;104:1685-1687.
10 +
Algvere PV, Hallnas K, Dafgard E, Hoog A.  Panretinal photocoagulation aggravates experimental proliferative vitreoretinopathy . Graefes Arch Clin Exp Ophthalmol . 1990;;228:461-466.
11 +
Campochiaro PA, Gaskin HC, Vinores SA.  Retinal cryopexy stimulates traction retinal detachment formation in the presence of an ocular wound . Arch Ophthalmol . 1987;;105:1567-1570.
12 +
Campochiaro PA, Jerdan JA, Glaser BM.  Serum contains chemoattractants for human retinal pigment epithelial cells . Arch Ophthalmol . 1984;;102:1830-1833.
13 +
Campochiaro PA, Glaser BM.  Platelet-derived growth factor is chemotactic for human retinal pigment epithelial cells . Arch Ophthalmol . 1985;;103:576-579.
14 +
Gauss-Muller V, Kleinman H, Martin GR, et al.  Role of attachment and attractants in fibroblast chemotaxis . J Lab Clin Med . 1980;;96:1071-1080.
15 +
de Juan E Jr, Dickson J, Hjelmeland L.  Serum is chemotactic for retinal-derived glial cells . Arch Ophthalmol . 1988;;106:986-990.
16 +
Cunha-Vaz JG.  The blood-ocular barriers . Surv Ophthalmol . 1979;;23:279-296.
17 +
Bito LZ, DeRousseau CJ.  Transport functions of the blood-retinal barrier system and the microenvironment of the retina . In: Cunha-Vaz JG, ed. The Blood-Retinal Barriers . New York, NY: Plenum Press; 1980;:133-163.
18 +
Conway BP.  Technical variables in vitreous fluorophotometry . Graefes Arch Clin Exp Ophthalmol . 1985;;222:194-201.
19 +
Plehwe WE, McRobbie DW, Lerski RA, Kohner EM.  Quantitative MRI in assessment of the blood-retinal barrier . Invest Ophthalmol Vis Sci . 1988;;29:663-670.
20 +
Berkowitz BA, Sato Y, Wilson DA, de Juan E Jr.  Blood retinal barrier breakdown investigated by real-time MRI following Gd-DTPA injection . Invest Ophthalmol Vis Sci . 1991;;32:2854-2860.
21 +
Sato Y, Berkowitz BA, Wilson CA, de Juan E Jr.  Blood-retinal barrier break-down caused by diode and argon laser endophotocoagulation: a comparative MRI study . Arch Ophthalmol . 1992;;110:277-281.
22 +
Berkowitz BA, Tofts P, Sen HA, Ando N, de Juan E Jr.  Accurate and precise measurement of blood-retinal barrier breakdown using dynamic Gd-DTPA MRI . Invest Ophthalmol Vis Sci . 1992;;33:3500-3506.
23 +
Sen HA, Berkowitz BA, Ando N, de Juan E Jr.  In vivo imaging of breakdown of the inner and outer blood-retinal barriers . Invest Ophthalmol Vis Sci . 1992;;33:3507-3512.
24 +
Sugita G, Tano Y, Machemer R, et al.  Intravitreal autotransplantation of fibroblasts . Am J Ophthalmol . 1980;;89:121-130.
25 +
Chandler DB, Hida T, Sheta S, et al.  Improvement in efficacy of corticosteroid therapy in an animal model of proliferative vitreoretinopathy by pretreatment . Graefes Arch Clin Exp Ophthalmol . 1987;;225:259-265.
26 +
Tano Y, Chandler D, Machemer R.  Treatment of intraocular proliferation with intravitreal injection of triamcinolone acetonide . Am J Ophthalmol . 1980;;90:810-816.
27 +
Wyatt JD, Scott RAW, Richardson ME.  The effect of prolonged ketamine-xylazine intravenous infusion on arterial blood pH, blood gases, mean arterial blood pressure, heart and respiratory rates, rectal temperature and reflexes in the rabbit . Lab Anim Sci . 1989;;39:411-416.
28 +
de Juan E Jr, Humayun M, Wilson D, Hatchell D.  Histopathology of experimental preretinal neovascularization . Invest Ophthalmol Vis Sci . 1989;;30:1495-1503.
29 +
de Juan E Jr, Wilson D, Hatchell D.  Breakdown of the blood-retinal barrier in a model of retinal neovascularization . Invest Ophthalmol Vis Sci . 1987;;28:1108-1115.
30 +
Hatchell DL, McAdoo T, Sheta S, et al.  Quantification of cellular proliferation in experimental proliferative vitreoretinopathy . Arch Ophthalmol . 1988;;106:669-672.
31 +
Fastenberg DM, Diddie KR, Dorey K, Ryan SJ.  The role of cellular proliferation in an experimental model of massive periretinal proliferation . Am J Ophthalmol . 1982;;93:565-572.
32 +
Tano Y, Sugita G, Abrams G, Machemer R.  Inhibition of intraocular proliferations with intravitreal corticosteroids . Am J Ophthalmol . 1980;;89:131-136.
33 +
McCuen BW, Bessler M, Tano Y, et al.  The lack of toxicity of intravitreally administered triamcinolone acetonide . Am J Ophthalmol . 1981;;91:785-788.
34 +
Ruhmann AG, Berliner DL.  Effect of steroids on growth of mouse fibroblasts in vitro . Endocrinology . 1965;;76:916-920.
35 +
Dannenberg AM.  The anti-inflammatory effects of glucocorticosteroids: a brief review of the literature . Inflammation . 1979;;3:329-343.
36 +
Blankenship GW.  Evaluation of a single intravitreal injection of dexamethasone phosphate in vitrectomy surgery for diabetic retinopathy complications . Graefes Arch Clin Exp Ophthalmol . 1991;;229:62-65.

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