Abstract
Capillary dropout is a critical process in diabetic retinopathy, resulting in ischemia, release of angiogenic growth factors, and sight-threatening retinal neovascularization.
It is essential to gain a greater understanding of this process in order to develop improved treatments for diabetic retinopathy. This chapter will review the organization, structure, and cellular composition of retinal capillaries. The histopathologic and clinical manifestations of capillary dropout in diabetic retinopathy will be discussed. Methods for detecting capillary dropout and experimental models for studying this phenomenon will be presented. Potential mechanisms for capillary dropout as well as contributory biochemical pathways will be discussed. Finally, the clinical consequences of capillary dropout will be summarized, highlighting the critical importance of this process in the pathophysiology of diabetic retinopathy.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Klein R, Klein BEK, Jensen SC, Moss SE. The relation of socioeconomics factors to the incidence of proliferative diabetic retinopathy and loss of vision. Ophthalmology 101, 68–76 (1994)
Chew EY. Epidemiology of diabetic retinopathy. Hosp Med 64, 396–399 (2003)
Engerman RL, Kern TS. Hyperglycemia as a cause of diabetic retinopathy. Metabolism 35(Suppl. 1), 20–23 (1986)
Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329, 977–986 (1993)
Porta M, Bandello F. Diabetic retinopathy: A clinical update. Diabetologia 45, 1617–1634 (2002)
Davis MD, Norton EWD, Myers FL. The Airlie House Classification of Diabetic Retinopathy, Washington, DC, 1969
Provis JM. Development of the primate retinal vasculature. Prog Retin Eye Res 20, 799–821 (2001)
Chan-Ling TL, Halasz P, Stone J. Development of retinal vasculature in the cat: Processes and mechanisms. Curr Eye Res 9, 459–478 (1990)
Michaelson IC. Vascular morphogenesis in the retina of the cat. . J Anat 82, 167–174 (1948)
Antonelli-Orlidge A, Smith SR, D'Amore PA. Influence of pericytes on capillary endothelial cell growth. Am Rev Respir Dis 140, 1129–1131 (1989)
Das A, Frank RN, Zhang NL, Samadini E. Increases in collagen type IV and laminin in galactose-induced retinal capillary basement membrane thickening-prevention by an aldose reductase inhibitor. Exp Eye Res 50, 269–280 (1990)
Shakib M, De Oliveira LF, Henkind P. Development of retinal vessels. II. Earliest stages of vessel formation. Invest Ophthalmol Vis Sci 7, 689–700 (1968)
Shakib M, Cunha-Vaz JG. Studies on the permeability of the blood–retinal barrier. I V. Junctional complexes of the retinal vessels and their role in the permeability of the blood-retinal barrier. Exp Eye Res 5, 229–234 (1966)
Gardner TW, Antonetti DA, Barber AJ, Lieth E, Tarbell JA. The molecular structure and function of the inner blood–retinal barrier. Documenta Ophthalmologica 97, 3–4 (1999)
Cunha-Vaz J, Faria de Abreu JR, Campos AJ. Early breakdown of the blood-retinal barrier in diabetes. Br J Ophthalmol 59, 649–656 (1975)
Kuwabara T, Cogan DG. Retinal vascular patterns. VI. Mural cells of retinal capillaries. Arch Ophthalmol 69, 492–502 (1963)
Hogan MJ, Feeney L. The ultrastructure of the retinal vessels. II. The small vessels. J Ultrastruc Res 49, 29–46 (1963)
Haefliger IO, Zschauer A, Anderson DR. Relaxation of retinal pericyte contractile tone through the nitric oxide-cyclic guanosine monophosphate pathway. Invest Ophthalmol Vis Sci 35, 991–997 (1994)
Hosoya K, Tomi M. Advances in the cell biology of transport via the inner blood—retinal barrier: Establishment of cell lines and transport functions. Biol Pharm Bull 28, 1–8 (2005)
Bresnick GH, Davis MD, Myers FL, de Venecia G. Clinicopathologic correlations in diabetic retin-opathy. II. Clinical and histologic appearances of retinal capillary microaneurysms. Arch Ophthalmol 95, 1215–1220 (1977)
Engerman RL. Pathogenesis of diabetic retinopathy. Diabetes 38, 1203–1206 (1989)
Mizutani M, Kern TS, Lorenzi M. Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J Clin Invest 97, 2883–2890 (1996)
Ashton N. Arteriolar involvement in diabetic retinopathy. Br J Ophthal 37, 282–292 (1953)
Engerman RL, Kern TS. Retinopathy in animal models of diabetes. Diabetes/Metabolism Rev 11, 109–120 (1995)
Niki T, Muraoka K, Shimizu K. Distribution of capillary nonperfusion in early-stage diabetic retin-opathy. Ophthalmology 91, 1431–1439 (1984)
Frank RN. Diabetic Retinopathy, Elsevier, Amsterdam, 1995
Frank RN. Diabetic Retinopathy. N Engl J Med 350, 48–58 (2004)
Engerman RL. Animal models of diabetic retinopathy. Trans Am Acad Ophthalmol Otolaryngol 81, 710–715 (1976)
Kohner EM, Dollery CT, Paterson JW, Oakley NW. Arterial fluorescein studies in diabetic retinopa-thy. Diabetes 16, 1–10 (1967)
Novotny HR, Alvis DL. A method of photographing fluorescence in circulating blood in the human retina. Circulation 24, 82–86 (1961)
Wessing A. Fluorescein appearance of the abnormal fundus. In: Meyer-Schwickerath G, ed. Fluorescein Angiography of the Retina, Mosby, Stuttgart, 1969, pp. 53–175
Schalnus R, Ohrloff C. The blood—ocular barrier in type I diabetes without diabetic retinopathy: Permeability measurements using fluorophotometry. Ophthalmic Res 27, 116–123 (1995)
Laatikainen L. The fluorescein angiography revolution: A breakthrough with sustained impact. Acta Ophthalmologica Scandinavica 82, 381–392 (2004)
Kohner EM, Henkind P. Correlation of fluorescein angiogram and retinal digest in diabetic retinopa-thy. Am J Ophthalmol 69, 403–414 (1970)
Ashton N. Studies of the retinal capillaries in relation to diabetic and other retinopathies. Br J Ophthalmol 47, 521–538 (1963)
Büchi RR, Kurosawa A, Tso MO. Retinopathy in diabetic hypertensive monkeys: A pathologic study. Graefes Arch Clin Exp Ophthalmol 234, 388–398 (1996)
Linsenmeier RA, Braun RD, McRipley MA, Padnick LB, Ahmed J, Hatchell DL, McLeod DS, Lutty GA. Retinal hypoxia in long-term diabetic cats. Invest Ophthalmol Vis Sci 39, 1647–1657 (1998)
Budzynski E, Wangsa-Wirawan N, Padnick-Silver L, Hatchell D, Linsenmeier R. Intraretinal pH in diabetic cats. Curr Eye Res 30, 229–240 (2005)
Engerman RL, Kramer JW. Dogs with induced or spontaneous diabetes as models for the study of human diabetes. Diabetes 31(Suppl. 1), 26–29 (1982)
Kern TS, Kowluru R, Engerman RL. Dog and rat models of diabetic retinopathy. In: Shafrir E, ed. Lessons from Animal Diabetes, Smith-Gordon, London, 1996, pp. 395–408
Kern TS, Engerman RL. Comparison of retinal lesions in alloxan-diabetic rats and galactose-fed rats. Curr Eye Res 13, 863–867 (1994)
Kern TS, Kowluru R, Engerman RL. Questions raised by study of experimental diabetic retinopathy. In: Kaneko SBaT, ed. Diabetes 1994; Proceedings of the 15th International Diabetes Federation Congress, Excerpta Medica, Kobe, Japan, 1995, pp. 331–334
Kern TS, Engerman RE. Animal model of human disease: A mouse model of diabetic retinopathy. Comp Pathol Bull 39, 3–6 (1997)
Beltramo E, Berrone E, Giunti S, Gruden G, Perin PC, Porta M. Effects of mechanical stress and high glucose on pericyte proliferation, apoptosis and contractile phenotype. Exp Eye Res 83, 989–994 (2006)
Kowluru RA, Kowluru V, Ho YS, Xiong Y. Overexpression of mitochondrial superoxide dismutase in mice protects the retina from diabetes-induced oxidative stress. Free Rad Biol Med 41, 1191–1196 (2006)
Kowluru RA, Kowluru A, Kanwar M. Small molecular weight G-protein, H-Ras, and retinal endothe-lial cell apoptosis in diabetes. Mol Cell Biochem 296, 69–76 (2007)
Miller AG, Smith DG, Bhat M, Nagaraj RH. Glyoxalase I is critical for human retinal capillary peri-cyte survival under hyperglycemic conditions. J Biol Chem 281, 11864–11871 (2006)
Mizutani M, Gerhardinger C, Lorenzi M. Muller cell changes in human diabetic retinopathy. Diabetes 47, 455–459 (1998)
Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest 102, 783–791 (1998)
Kern TS, Tang J, Mizutani M, Kowluru R, Nagraj R, Lorenzi M. Response of capillary cell death to aminoguanidine predicts the development of retinopathy: Comparison of diabetes and galactosemia. Invest Ophthalmol Vis Sci 41, 3972–3978 (2000)
Barber AJ, Antonetti DA, Kern TS, Reiter CE, Soans RS, Krady JK, Levison SW, Gardner TW, Bronson SK. The Ins2Akita mouse as a model of early retinal complications in diabetes. Invest Ophthalmol Vis Sci 46, 2210–2218 (2005)
Barile GR, Pachydaki SI, Tari SR, Lee SE, Donmoyer CM, Ma W, Rong LL, Buciarelli LG, Wendt T, Hörig H, Hudson BI, Qu W, Weinberg AD, Yan SF, Schmidt AM. The RAGE axis in early diabetic retinopathy. Invest Ophthalmol Vis Sci 46, 2916–2924 (2005)
Feit-Leichman RA, Kinouchi R, Takeda M, Fan Z, Mohr S, Kern TS, Chen DF. Vascular damage in a mouse model of diabetic retinopathy: Relation to neuronal and glial changes. Invest Ophthal Vis Sci 46, 4281–4287 (2005)
Kuwabara T, Cogan DG. Retinal vascular patterns. VII. Acellular change. Invest Ophthalmol Vis Sci 4, 1049–1064 (1965)
Kador PF, Akagi Y, Terubayashi H, Wyman M, Kinoshita JH. Prevention of pericyte ghost formation in retinal capillaries of galactose-fed dogs by aldose reductase inhibitors. Arch Ophthalmol 106, 1099–1102 (1988)
Engerman RL, Pfaffenbach D, Davis MD. Cell turnover of capillaries. Lab Invest 17, 738–743 (1967)
Kowluru RA, Koppolu P. Diabetes-induced activation of caspase-3 in retina: Effect of antioxidant therapy. Free Radic Res 36, 993–999 (2002)
Kowluru RA, Odenbach S. Effect of long-term administration of alpha lipoic acid on retinal capillary cell death and the development of retinopathy in diabetic rats. Diabetes 53, 3233–3238 (2004)
Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD. Programmed cell death and the control of cell survival: Lessons from the nervous system. Science 262, 695–700 (1993)
Cogan DG, Toussaint D, Kuwabara T. Retinal vascular patterns. I V. Diabetic retinopathy. Arch Ophthalmol 66, 366–378 (1961)
Dodge AB, D'Amore PA. Cell—cell interactions in diabetic angiopathy. Diabetes Care 15, 1168–1180 (1992)
Murata M, Ohta N, Fujisawa S, Tsai JY, Sato S, Akagi Y, Takahashi Y, Neuenschwander H, Kador PF. Selective pericyte degeneration in the retinal capillaries of galactose-fed dogs results from apop-tosis linked to aldose reductase-catalyzed galactitol accumulation. J Diabetes Complicat 16, 363–370 (2002)
Gardiner TA, Archer DB, Curtis TM, Stitt AW. Arteriolar involvement in the microvascular lesions of diabetic retinopathy: Implications for pathogenesis. Microcirculation 14, 25–38 (2007)
Sharma AK, Gardiner TA, Archer DB. A morphologic and autoradiographic study of cell death and regeneration in the retinal microvasculature of normal and diabetic rats. Am J Ophthalmol 100, 51–60 (1985)
Hammes HP, Lin J, Bretzel RG, Brownlee M, Breier G. Upregulation of the vascular endothelial growth factor/vascular endothelial growth factor receptor sysytem in experimental background diabetic retinopathy of the rats. Diabetes 47, 401–406 (1998)
Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 37, 614–636 (1965)
Linskens MH, Harley CB, West MD, Campisi J, Hayflick L. Replicative senescence and cell death. Science 267, 17 (1995)
Joussen AM, Murata T, Tsujikawa A, Kirchhof B, Bursell SE, Adamis AP. Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol 158, 147–152 (2001)
Joussen AM, Poulaki V, Le ML, Koizumi K, Esser C, Janicki H, Schraermeyer U, Kociok N, Fauser S, Kirchhof B, Kern TS, Adamis AP. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J 18, 1450–1452 (2004)
Kowluru RA, Odenbach S. Role of interleukin-1beta in the pathogenesis of diabetic retinopathy. Br J Ophthalmol 88, 1343–1347 (2004)
Kowluru RA, Odenbach S. Role of interleukin-1beta in the development of retinopathy in rats: Effect of antioxidants. Invest Ophthalmol Vis Sci 45, 4161–4166 (2004)
Kern TS, Miller CM, Du Y, Zheng L, Mohr S, Ball SL, Kim M, Jamison JA, Bingaman DP. Topical administration of nepafenac inhibits diabetes-induced retinal microvascular disease and underlying abnormalities of retinal metabolism and physiology. Diabetes 56, 373–379 (2007)
Kaji Y, Usui T, Ishida S, Yamashiro K, Moore TC, Moore J, Yamamoto Y, Yamamoto H, Adamis AP. Inhibition of diabetic leukostasis and blood—retinal barrier breakdown with a soluble form of a receptor for advanced glycation end products. Invest Ophthalmol Vis Sci 48, 858–865 (2007)
Carmo A, Cunha-Vaz JG, Carvalho A P, Lopes MC. L-arginine transport in retinas from streptozotocin diabetic rats: Correlation with the level of IL-1 beta and NO synthase activity. Vision Res 39, 3817– 3823 (1999)
Yuuki T, Kanda T, Kimura Y, Kotajima N, Tamura J, Kobayashi I, Kishi S. Inflammatory cytokines in vitreous fluid and serum of patients with diabetic vitreoretinopathy. J Diabetes Complicat 15, 257–259 (2001)
Zheng L, Gong B, Hatala DA, Kern TS. Retinal ischemia and reperfusion causes capillary degeneration: Similarities to diabetes. Invest Ophthalmol Vis Sci 48, 361–367 (2007)
Joussen AM, Poulaki V, Mitsiades N, Cai W Y, Suzuma I, Pak J, Ju ST, Rook SL, Esser P, Mitsiades CS, Kirchhof B, Adamis AP, Aiello LP. Suppression of Fas-FasL-induced endothelial cell apoptosis prevents diabetic blood—retinal barrier breakdown in a model of streptozotocin-induced diabetes. FASEB J 17, 76–78 (2003)
Kociok N, Radetzky S, Krohne TU, Gavranic C, Joussen AM. Pathological but not physiological retinal neovascularization is altered in TNF-Rp55-receptor-deficient mice. Invest Ophthalmol Vis Sci 47, 5057–5065 (2006)
Naveh-Floman N, Weissman C, Belkin M. Arachidonic acid metabolism by retinas of rats with streptozotocin-induced diabetes. Curr Eye Res 3, 1135–1139 (1984)
Johnson EI, Dunlop ME, Larkins RG. Increased vasodilatory prostaglandin production in the diabetic rat retinal vasculature. Curr Eye Res 18, 79–82 (1999)
Joussen AM, Poulaki V, Mitsiades N, Kirchhof B, Koizumi K, Dohmen S, Adamis A P. Nonsteroidal anti-inflammatory drugs prevent early diabetic retinopathy via TNF-alpha suppression. FASEB J 16, 438–440 (2002)
Ayalasomayajula SP, Kompella UB. Celecoxib, a selective cyclooxygenase-2 inhibitor, inhibits retinal vascular endothelial growth factor expression and vascular leakage in a streptozotocin-induced diabetic rat model. Eur J Pharmacol 458, 283–289 (2003)
Du Y, Sarthy VP, Kern TS. Interaction between NO and COX pathways in retinal cells exposed to elevated glucose and retina of diabetic rats. Am J Physiol Regul Integr Comp Physiol 287, R734–R741 (2004)
Kowluru RA, Engerman RL, Kern TS. Abnormalities of retinal metabolism in diabetes or experimental galactosemia VIII. Prevention by aminoguanidine. Curr Eye Res 21, 814–819 (2000)
Kowluru RA, Tang J, Kern TS. Abnormalities of retinal metabolism in diabetes and experimental galactosemia. VII. Effect of long-term administration of antioxidants on the development of retinopa-thy. Diabetes 50, 1938–1942 (2001)
Abu El-Asrar AM, Desmet S, Meersschaert A, Dralands L, Missotten L, Geboes K. Expression of the inducible isoform of nitric oxide synthase in the retinas of human subjects with diabetes mellitus. Am J Ophthalmol 132, 551–556 (2001)
Du Y, Smith MA, Miller CM, Kern TS. Diabetes-induced nitrative stress in the retina, and correction by aminoguanidine. J Neurochem 80, 771–779 (2002)
Kowluru RA. Effect of re-institution of good glycemic control on retinal oxidative stress and nitrative stress in diabetic rats. Diabetes 52, 818–823 (2003)
Kowluru RA, Kanwar M, Kennedy A. Metabolic memory phenomenon and accumulation of perox-ynitrite in retinal capillaries. Exp Diabetes Res 2007, 1–7 (2007)
Zheng L, Du Y, Miller C, Gubitosi-Klug RA, Kern TS, Ball S, Berkowitz BA. Critical role of induc-ible nitric oxide synthase in degeneration of retinal capillaries in mice with streptozotocin-induced diabetes. Diabetologia 50, 1987–1996 (2007)
Lee JI, Burckart GJ. Nuclear factor kappa B: Important transcription factor and therapeutic target. J Clin Pharmacol 38, 981–993 (1998)
Romeo G, Liu WH, Asnaghi V, Kern TS, Lorenzi M. Activation of nuclear factor-kappaB induced by diabetes and high glucose regulates a proapoptotic program in retinal pericytes. Diabetes 51, 2241– 2248 (2002)
Kowluru RA, Koppolu P, Chakrabarti S, Chen S. Diabetes-induced activation of nuclear transcrip-tional factor in the retina, and its inhibition by antioxidants. Free Radic Res 37, 1169–1180 (2003)
Kowluru RA, Chakrabarti S, Chen S. Re-Institution of good metabolic control in diabetic rats on the activation of caspase-3 and nuclear transcriptional factor (NF-kB) in the retina. Acta Diabetologica 44, 194–199 (2004)
Zheng L, Szabo C, Kern TS. Poly(ADP-ribose) polymerase is involved in the development of diabetic retinopathy via regulation of nuclear factor-kappaB. Diabetes 53, 2960–2967 (2004)
Zheng L, Howell SJ, Hatala DA, Huang K, Kern TS. Salicylate-based anti-inflammatory drugs inhibit the early lesion of diabetic retinopathy. Diabetes 56, 337–345 (2007)
Barile GR, Chang SS, Park LS, et al. Soluble cellular adhesion molecules in proliferative vitreoretin-opathy and proliferative diabetic retinopathy. Curr Eye Res 19, 219–227 (1999)
Matsumoto K, Sera Y, Ueki Y, Inukai G, Niiro E, Miyake S. Comparison of serum concentrations of soluble adhesion molecules in diabetic microangiopathy and macroangiopathy. Diabet Med 19, 822–826 (2002)
van Hecke MV, Dekker JM, Nijpels G, Moll AC, Heine RJ, Bouter LM, Polak BC, Stehouwer CD. Inflammation and endothelial dysfunction are associated with retinopathy: The Hoorn Study. Diabetologia 48, 1300–1306 (2005)
Osborn L. Leukocyte adhesion to endothelium in inflammation. Cell 62, 3–6 (1990)
Matsuoka M, Ogata N, Minamino K, Matsumura M. Leukostasis and pigment epithelium-derived factor in rat models of diabetic retinopathy. Mol Vis 13, 1058–1065 (2007)
Schröder S, Palinski W, Schmid-Schönbein GW. Activated monocytes and granulocytes, capillary nonperfusion, and neovascularization in diabetic retinopathy. Am J Pathol 139, 81–100 (1991)
Miyamoto K, Khosrof S, Busell SE, Rohan R, Murata T, Clermont AC, Aiello LP, Ogura Y, Adamis AP. Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci USA 96, 10836– 10841 (1999)
Moore TC, Moore JE, Kaji Y, Frizzell N, Usui T, Poulaki V, Campbell IL, Stitt AW, Gardiner TA, Archer DB, Adamis AP. The role of advanced glycation end products in retinal microvascular leuko-stasis. Invest Ophthalmol Vis Sci 44, 4457–4464 (2003)
Miyamoto K, Ogura Y. Pathogenetic potential of leukocytes in diabetic retinopathy. Sem in Ophthalmol 14, 233–239 (1999)
Hossain P. Scanning laser ophthalmoscopy and fundus fluorescent leucocyte angiography. Br J Ophthalmol 83, 1250–1253 (1999)
Boeri D, Maiello M, Lorenzi M. Increased prevalence of microthromboses in retinal capillaries of diabetic individuals. Diabetes 50, 1432–1439 (2001)
Yamagishi S, Yamamoto Y, Harada S, Hsu CC, Yamamoto H. Advanced glycosylation end products stimulate the growth but inhibit the prostacyclin-producing ability of endothelial cells through interactions with their receptors. FEBS Lett 384, 103–106 (1996)
Yamagishi S, Fujimori H, Yonekura H, Yamamoto Y, Yamamoto H. Advanced glycation endproducts inhibit prostacyclin production and induce plasminogen activator inhibitor-1 in human microvascular endothelial cells. Diabetologia 41, 1435–1441 (1998)
Ishibashi T, Tanaka K, Taniguchi Y. Platelet aggregation and coagulation in the pathogenesis of diabetic retinopathy in rats. Diabetes 30, 601–605 (1981)
Sima AAF, Chakrabarti S, Garcia-Salinas R, Basu PK. The BB-rat: An authentic model of human diabetic retinopathy. Curr Eye Res 4, 1087–1092 (1985)
Stitt AW. The role of advanced glycation in the pathogenesis of diabetic retinopathy. Exp Mol Pathol 75, 95–108 (2003)
Kowluru RA. Effect of advanced glycation end products on accelerated apoptosis of retinal capillary cells under in vitro conditions. Life Sci 76, 1051–1060 (2005)
Baynes JW, Thrope SR. Role of oxidative stress in diabetic complications: A new perspective on an old paradigm. Diabetes 48, 1–9 (1999)
Du XL, Edelstein D, Rossetti L, Fantus IG, Goldberg H, Ziyadeh F, Wu J, Brownlee M. Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc Natl Acad Sci 97, 12222–12226 (2000)
Baumgartner-Parzer SM, Wagner L, Pettermann M, Grillari J, Gessl A, Waldhausl W. High-glucose-triggered apoptosis in cultured endothelial cells. Diabetes 44, 1323–1327 (1995)
Brownlee M. The pathobiology of diabetic complications: A unifying mechanism. Diabetes 54, 1615– 1625 (2005)
Kanwar M, Chan PS, Kern TS, Kowluru RA. Oxidative damage in the retinal mtochondria of diabetic mice: Possible protection by superoxide dismutase. Invest Ophthalmol Vis Sci 48, 3805–3811 (2007)
Arend O, Wolf S, Harris A, Reim M. The relationship of macular microcirculation to visual acuity in diabetic patients. Arch Ophthalmol 113, 610–614 (1995)
Bresnick GH, Condit R, Syrjala S, Palta M, Groo A, Korth K. Abnormalities of the foveal avascular zone in diabetic retinopathy. Arch Ophthalmol 102, 1286–1293 (1984)
Arend O, Wolf S, Jung F, Bertram B, Pöstgens H, Toonen H, Reim M. Retinal microcirculation in patients with diabetes mellitus: Dynamic and morphological analysis of perifoveal capillary network. Br J Ophthalmol 75, 514–518 (1991)
Arend O, Remky A, Evans D, Stüber R, Harris A. Contrast sensitivity loss is coupled with capillary dropout in patients with diabetes. Invest Ophthalmol Vis Sci 38, 1819–1824 (1997)
Hickman JB, Frayser R. Studies of the retinal circulation in man: Observations on vessel diameter, arteriovenous oxygen difference, and mean circulation time. Circulation 33, 302–316 (1966)
Kristinsson JK, Gottfredsdóttir MS, Stefánsson E. Retinal vessel dilatation and elongation precedes diabetic macular oedema. Br J Ophthalmol 81, 274–278 (1997)
Golubovic-Arsovska M. Correlation of diabetic maculopathy and level of diabetic retinopathy. Prilozi 27, 139–150 (2006)
Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus. JAMA 287, 2563–2569 (2002)
Diabetes Control and Complications Trial Research Group. Hypoglycemia in the diabetes control and complications trial. Diabetes 46, 271–286 (1997)
Acknowledgments
Authors would like to thank Dr. T. S. Kern and Dr. R. N. Frank for providing the patient pictures included in this chapter and Mamta Kanwar for technical help. The studies from our laboratory reported here were supported in part by research grants from the National Institutes of Health, the Juvenile Diabetes Foundation International, and by a departmental unrestricted grant from Research to Prevent Blindness.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2008 Humana Press, a part of Springer Science + Business Media, LLC
About this chapter
Cite this chapter
Kowluru, R.A., Chan, PS. (2008). Capillary Dropout in Diabetic Retinopathy. In: Duh, E.J. (eds) Diabetic Retinopathy. Contemporary Diabetes. Humana Press. https://doi.org/10.1007/978-1-59745-563-3_11
Download citation
DOI: https://doi.org/10.1007/978-1-59745-563-3_11
Publisher Name: Humana Press
Print ISBN: 978-1-934115-83-1
Online ISBN: 978-1-59745-563-3
eBook Packages: MedicineMedicine (R0)