Ocular oxygenation and the treatment of diabetic retinopathy.

Retinal photocoagulation and vitrectomy both reduce diabetic macular edema and neovascularization in diabetic retinopathy. We suggest that this clinical effect is based on the effect these treatment modalities have on retinal oxygenation, and we present a theory to explain why retinal photocoagulation and vitrectomy influence edema and neovascularization in diabetic and other ischemic retinopathies.

[1]  M. Tso,et al.  Experimental photocoagulation of the human retina. II. Electron microscopic study. , 1977, Archives of ophthalmology.

[2]  E. Stefánsson,et al.  VITRECTOMY, LENSECTOMY, AND OCULAR OXYGENATION , 1982, Retina.

[3]  L'esperance Fa The treatment of ophthalmic vascular disease by argon laser photocoagulation , 1969 .

[4]  Tomohiro Otani,et al.  Resolution of diabetic cystoid macular edema associated with spontaneous vitreofoveal separation. , 2003, American journal of ophthalmology.

[5]  I. Morita,et al.  Stimulatory effects of insulin and insulin-like growth factor I on migration and tube formation by vascular endothelial cells. , 1992, Atherosclerosis.

[6]  D. Foreman,et al.  VEGF localisation in diabetic retinopathy , 1998, The British journal of ophthalmology.

[7]  S. Nicosia,et al.  Vascular endothelial growth factor, platelet-derived growth factor, and insulin-like growth factor-1 promote rat aortic angiogenesis in vitro. , 1994, The American journal of pathology.

[8]  K. Suzuma,et al.  Hypoxia and Vascular Endothelial Growth Factor Selectively Up-regulate Angiopoietin-2 in Bovine Microvascular Endothelial Cells* , 1999, The Journal of Biological Chemistry.

[9]  F. Ferris,et al.  Optic disk neovascularization and retinal vessel diameter in diabetic retinopathy. , 1988, American journal of ophthalmology.

[10]  W. Benedict,et al.  Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. , 1999, Science.

[11]  M. Boulton,et al.  Production of IGF-I and IGF binding proteins by retinal cells in vitro. , 1994, The British journal of ophthalmology.

[12]  Reginald Birngruber,et al.  Threshold determinations for selective retinal pigment epithelium damage with repetitive pulsed microsecond laser systems in rabbits. , 2002, Ophthalmic surgery and lasers.

[13]  J. Livesey,et al.  Measurement and manipulation of the partial pressure of oxygen in the rat anterior chamber , 2000, Current eye research.

[14]  R. Kelly,et al.  Harnessing the response to tissue hypoxia: HIF-1 alpha and therapeutic angiogenesis. , 2002, Trends in cardiovascular medicine.

[15]  P Massin,et al.  Growth factors and diabetic retinopathy. , 1997, Diabetes & metabolism.

[16]  A. Ljubimov,et al.  Effects of angiogenic growth factor combinations on retinal endothelial cells. , 2002, Experimental eye research.

[17]  R G Allen,et al.  Retinal damage from long-term exposure to laser radiation. , 1977, Investigative ophthalmology & visual science.

[18]  L. Aiello,et al.  Cyclic stretch and hypertension induce retinal expression of vascular endothelial growth factor and vascular endothelial growth factor receptor-2: potential mechanisms for exacerbation of diabetic retinopathy by hypertension. , 2001, Diabetes.

[19]  J. Folkman,et al.  Hypoxic Induction of Endothelial Cell Growth Factors in Retinal Cells: Identification and Characterization of Vascular Endothelial Growth Factor (VEGF) as the Mitogen , 1995 .

[20]  E. Stefánsson,et al.  Retinal vasoconstriction after laser treatment for diabetic macular edema. , 1993, American journal of ophthalmology.

[21]  G. Lip,et al.  Plasma VEGF and soluble VEGF receptor FLT-1 in proliferative retinopathy: relationship to endothelial dysfunction and laser treatment. , 2000, Investigative ophthalmology & visual science.

[22]  R. Miech,et al.  Effects of laser photocoagulation on adenine nucleotides in rabbit retinas. , 1976, Archives of ophthalmology.

[23]  S. Riaskoff Photocoagulation treatment of proliferative diabetic retinopathy. , 1981, Bulletin de la Societe belge d'ophtalmologie.

[24]  R. Holman,et al.  Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. , 1998 .

[25]  D. Foreman,et al.  Immunolocalisation of the VEGF receptors FLT-1, KDR, and FLT-4 in diabetic retinopathy , 1999, The British journal of ophthalmology.

[26]  N. Blair,et al.  Ocular oxygen consumption during vitreoperfusion in the cat. , 2000, Transactions of the American Ophthalmological Society.

[27]  E. Keshet,et al.  Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis , 1992, Nature.

[28]  J. Weiter,et al.  The influence of the photoreceptor-RPE complex on the inner retina. An explanation for the beneficial effects of photocoagulation. , 1980, Ophthalmology.

[29]  Effects of oxygen and carbon dioxide on human retinal circulation: an investigation using blue field simulation and scanning laser ophthalmoscopy. , 2005, Acta ophthalmologica Scandinavica.

[30]  N. Bouck,et al.  Prevention of ischemia-induced retinopathy by the natural ocular antiangiogenic agent pigment epithelium-derived factor , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  J. Rubin,et al.  Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. , 1991, Science.

[32]  Daniel B. Rifkin,et al.  Fibroblast Growth Factor-2 (FGF-2) Induces Vascular Endothelial Growth Factor (VEGF) Expression in the Endothelial Cells of Forming Capillaries: An Autocrine Mechanism Contributing to Angiogenesis , 1998, The Journal of cell biology.

[33]  L. Aiello,et al.  Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. , 1994, The New England journal of medicine.

[34]  R Machemer,et al.  Retinal oxygenation and laser treatment in patients with diabetic retinopathy. , 1992, American journal of ophthalmology.

[35]  B. Bertram,et al.  Retinale Gefäße vor und nach Photokoagulation bei diabetischer Retinopathie - Durchmesserbestimmungen mittels digitalisierter Farbdiapositive , 1996 .

[36]  L. Jampol Oxygen therapy and intraocular oxygenation. , 1987, Transactions of the American Ophthalmological Society.

[37]  Quan Dong Nguyen,et al.  Supplemental oxygen improves diabetic macular edema: a pilot study. , 2004, Investigative ophthalmology & visual science.

[38]  L. Laatikainen,et al.  Long‐term visual results of vitreous surgery in diabetic eye disease , 1989, Acta ophthalmologica.

[39]  J. McLaren,et al.  Measuring oxygen tension in the anterior chamber of rabbits. , 1998, Investigative ophthalmology & visual science.

[40]  T. Nakamura,et al.  Inhibitory effect of hepatocyte growth factor against FaO hepatocellular carcinoma cells may be associated with changes of intracellular signalling pathways mediated by protein kinase C. , 1994, Research communications in molecular pathology and pharmacology.

[41]  J. Caro,et al.  Hypoxia regulatory elements of the human vascular endothelial growth factor gene. , 1994, Cellular & molecular biology research.

[42]  E. Stefánsson,et al.  Quantitative measurements of retinal edema by specific gravity determinations. , 1987, Investigative ophthalmology & visual science.

[43]  M. Larsen,et al.  Unilateral diabetic macular oedema secondary to central retinal vein congestion. , 2004, Acta ophthalmologica Scandinavica.

[44]  G N Foulks,et al.  The effect of corneal contact lenses on the oxygen tension in the anterior chamber of the rabbit eye. , 1987, Investigative ophthalmology & visual science.

[45]  M L Wolbarsht,et al.  Increased retinal oxygen supply following pan-retinal photocoagulation and vitrectomy and lensectomy. , 1981, Transactions of the American Ophthalmological Society.

[46]  Colin T. Dollery,et al.  The Retinal Circulation , 1972 .

[47]  M. Larsen,et al.  Diabetic macular oedema: the effect of photocoagulation on fluorescein transport across the blood-retinal barrier , 2002, The British journal of ophthalmology.

[48]  Y. Ogura,et al.  Alterations of retinal microcirculation in response to scatter photocoagulation. , 1998, Investigative ophthalmology & visual science.

[49]  A. Mendívil,et al.  OCULAR BLOOD FLOW VELOCITIES IN PATIENTS WITH PROLIFERATIVE DIABETIC RETINOPATHY AFTER SCATTER PHOTOCOAGULATION: Two Years of Follow-Up , 1996, Retina.

[50]  G. Bresnick,et al.  Ocular effects of argon laser radiation. II. Histopathology of chorioretinal lesions. , 1971, American journal of ophthalmology.

[51]  C. A. Wilson,et al.  Transcorneal oxygenation of the preretinal vitreous. , 1994, Archives of ophthalmology.

[52]  J. Simons,et al.  Hypoxia-inducible factor 1α and 1β proteins share common signaling pathways in human prostate cancer cells , 2001 .

[53]  C. H. Chen,et al.  Vascular endothelial cell effectors in fetal calf retina, vitreous, and serum. , 1982, Investigative ophthalmology & visual science.

[54]  V. Han,et al.  Modulation of insulin-like growth factor (IGF) and IGF binding protein biosynthesis by hypoxia in cultured vascular endothelial cells. , 1998, The Journal of endocrinology.

[55]  O. Hudlická Is Physiological Angiogenesis in Skeletal Muscle Regulated by Changes in Microcirculation? , 1998, Microcirculation.

[56]  M. Larsen,et al.  Overnight thickness variation in diabetic macular edema. , 2005, Investigative ophthalmology & visual science.

[57]  R. Iezzi,et al.  Temporal variation in diabetic macular edema measured by optical coherence tomography. , 2004, Ophthalmology.

[58]  O. Hudlická THE BENJAMIN W. ZWEIFACH AWARD LECTURE 1997 , 1998 .

[59]  R. Simó,et al.  Vitreous levels of IGF-I, IGF binding protein 1, and IGF binding protein 3 in proliferative diabetic retinopathy: a case-control study. , 2000, Diabetes care.

[60]  H. Zhu,et al.  Yeast flavohemoglobin is an ancient protein related to globins and a reductase family. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[61]  A. Patz,et al.  Studies on retinal neovascularization. Friedenwald Lecture. , 1980, Investigative ophthalmology & visual science.

[62]  N. Osborne,et al.  Retinal ischemia: mechanisms of damage and potential therapeutic strategies , 2004, Progress in Retinal and Eye Research.

[63]  R. Linsenmeier,et al.  Retinal hypoxia in long-term diabetic cats. , 1998, Investigative ophthalmology & visual science.

[64]  B. Petrig,et al.  Retinal blood flow regulation and the clinical response to panretinal photocoagulation in proliferative diabetic retinopathy. , 1989, Ophthalmology.

[65]  Curtis L. Meinert,et al.  Photocoagulation treatment of proliferative diabetic retinopathy: the second report of diabetic retinopathy study findings. , 1978, Ophthalmology.

[66]  M. Boulton,et al.  Increased expression of placenta growth factor in proliferative diabetic retinopathy. , 1998, Laboratory investigation; a journal of technical methods and pathology.

[67]  A. Jalkh,et al.  Comparative study of vitreoretinal relationships using biomicroscopy and ultrasound , 1991, Graefe's Archive for Clinical and Experimental Ophthalmology.

[68]  H. Yamashita,et al.  Expression of placenta growth factor (PIGF) in ischaemic retinal diseases , 1999, Eye.

[69]  L. Cantley,et al.  The tyrosine-phosphorylated hepatocyte growth factor/scatter factor receptor associates with phosphatidylinositol 3-kinase. , 1991, The Journal of biological chemistry.

[70]  D. Faller,et al.  Oxygen tension regulates the expression of the platelet-derived growth factor-B chain gene in human endothelial cells. , 1990, The Journal of clinical investigation.

[71]  V. Hessemer,et al.  Influence of panretinal photocoagulation on the ocular pulse curve. , 1997, American journal of ophthalmology.

[72]  J Strobel,et al.  Multisubstance Analysis of Reflection Spectra before and after Laser Photocoagulation for Proliferative Diabetic Retinopathy , 1997, European journal of ophthalmology.

[73]  E. Stefánsson,et al.  Vasodilation and the etiology of diabetic retinopathy: a new model. , 1981, Ophthalmic surgery.

[74]  W. Green,et al.  Response of pig retinal pigment epithelium to laser photocoagulation in organ culture. , 1989, Archives of ophthalmology.

[75]  P. Campochiaro,et al.  Angiopoietin 2 expression in the retina: upregulation during physiologic and pathologic neovascularization , 2000, Journal of cellular physiology.

[76]  J. Mellerio,et al.  Pathological development of retinal laser photocoagulations. , 1967, Experimental eye research.

[77]  M. Tsacopoulos,et al.  Effect of laser photocoagulation on oxygenation of the retina in miniature pigs. , 1985, Investigative ophthalmology & visual science.

[78]  H. Zhu,et al.  Oxygen sensing and signaling: impact on the regulation of physiologically important genes. , 1999, Respiration physiology.

[79]  Einar Stefánsson,et al.  Retinal vessel dilatation and elongation precedes diabetic macular oedema , 1997, The British journal of ophthalmology.

[80]  G. Semenza Expression of hypoxia-inducible factor 1: mechanisms and consequences. , 2000, Biochemical pharmacology.

[81]  J. Jonas Intravitreal triamcinolone acetonide for treatment of intraocular oedematous and neovascular diseases. , 2005, Acta ophthalmologica Scandinavica.

[82]  M. Kondo,et al.  Changes in focal macular electroretinograms and foveal thickness after vitrectomy for diabetic macular edema. , 2003, Investigative ophthalmology & visual science.

[83]  M. Aoki,et al.  Potential Role of an Endothelium-Specific Growth Factor, Hepatocyte Growth Factor, on Endothelial Damage in Diabetes , 1997, Diabetes.

[84]  T Bek,et al.  Diabetic maculopathy caused by disturbances in retinal vasomotion. A new hypothesis. , 1999, Acta ophthalmologica Scandinavica.

[85]  V. Suomalainen Comparison of retinal lesions produced by transscleral krypton laser photocoagulation, transpupillar krypton laser photocoagulation and cryocoagulation , 1993, Acta ophthalmologica.

[86]  N. Fausto Hepatocyte growth factor receptor and the c-met oncogene Bottaro DP, Rubin JS, Faletto DL, Chan AM-L, Kmiecik TE, Vande Woude GF, Aaronson SA. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 1991;251:802?804 , 1991 .

[87]  V. Caviness,et al.  HEMORRHAGES INTO PERIPHERAL NERVES IN ASSOCIATION WITH LEUKEMIA. , 1964 .

[88]  Ic. Michaelson,et al.  The mode of development of the vascular system of the retina, with some observations on its significance for certain retinal diseases , 1948 .

[89]  T. Yamamoto,et al.  Vitrectomy for diabetic macular edema: the role of posterior vitreous detachment and epimacular membrane. , 2001, American journal of ophthalmology.

[90]  M L Wolbarsht,et al.  PANRETINAL PHOTOCOAGULATION AND RETINAL OXYGENATION , 1982, Retina.

[91]  P. Campochiaro,et al.  Hypoxia inducible factor-1alpha is increased in ischemic retina: temporal and spatial correlation with VEGF expression. , 1999, Investigative ophthalmology & visual science.

[92]  H. Hammes,et al.  Loss of the antiangiogenic pigment epithelium-derived factor in patients with angiogenic eye disease. , 2001, Diabetes.

[93]  M. Tsacopoulos,et al.  Scatter photocoagulation restores tissue hypoxia in experimental vasoproliferative microangiopathy in miniature pigs. , 1990, Ophthalmology.

[94]  P. Wiedemann,et al.  Basic fibroblast growth factor mRNA, bFGF peptide and FGF receptor in epiretinal membranes of intraocular proliferative disorders (PVR and PDR) , 1997, International Ophthalmology.

[95]  C. Pournaras,et al.  RETINAL OXYGEN DISTRIBUTION: Its Role in the Physiopathology of Vasoproliferative Microangiopathies , 1995, Retina.

[96]  R. Birngruber,et al.  [Histology of retinal lesions after continuous irradiation and selective micro-coagulation of the retinal pigment epithelium]. , 1993, Der Ophthalmologe : Zeitschrift der Deutschen Ophthalmologischen Gesellschaft.

[97]  U. Kellner,et al.  Oxygen in the anterior chamber of the human eye. , 1993, German journal of ophthalmology.

[98]  M. Goldberg,et al.  Transcriptional Regulation of the Rat Vascular Endothelial Growth Factor Gene by Hypoxia (*) , 1995, The Journal of Biological Chemistry.

[99]  G. Blankenship,et al.  Pars plana vitrectomy for the management of severe diabetic retinopathy: an analysis of results five years following surgery. , 1978, Ophthalmology.

[100]  J. Erusalimsky,et al.  Basic fibroblast growth factor upregulates the expression of vascular endothelial growth factor in vascular smooth muscle cells. Synergistic interaction with hypoxia. , 1995, Circulation.

[101]  J. Caro,et al.  Hypoxia regulation of gene transcription. , 2001, High altitude medicine & biology.

[102]  A. Mendívil Ocular blood flow velocities in patients with proliferative diabetic retinopathy after panretinal photocoagulation. , 1997, Survey of ophthalmology.

[103]  G D Frisch,et al.  Recovery of the retina from argon laser radiation: clinical and light microscopic evaluation. , 1974, Annals of ophthalmology.

[104]  Pournaras Cj,et al.  Occlusions vasculaires rétiniennes: les possibilités d'apport direct d'oxygène dans les territoires hypoxiques , 1985 .

[105]  H. Shimokawa,et al.  Induction of vascular endothelial growth factor after application of mechanical stress to retinal pigment epithelium of the rat in vitro. , 1999, Investigative ophthalmology & visual science.

[106]  A. Giaccia,et al.  Induction of vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/Akt signaling pathway in Ha-ras-transformed cells through a hypoxia inducible factor-1 transcriptional element. , 1997, Blood.

[107]  I. C. Michaelson,et al.  Effect of Increased Oxygen on the Development of the Retinal Vessels * , 1954, The British journal of ophthalmology.

[108]  F Hillenkamp,et al.  Microphotocoagulation: selective effects of repetitive short laser pulses. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[109]  J. Robertson,et al.  Platelet-derived growth factor ligands and receptors immunolocalized in proliferative retinal diseases. , 1994, Investigative ophthalmology & visual science.

[110]  P. Ratcliffe,et al.  Oxygen sensors and angiogenesis. , 2002, Seminars in cell & developmental biology.

[111]  L. Giudice,et al.  Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[112]  R Machemer,et al.  Panretinal photocoagulation and retinal oxygenation in normal and diabetic cats. , 1986, American journal of ophthalmology.

[113]  E. Kohner,et al.  A two-year follow-up study of serum insulinlike growth factor-I in diabetics with retinopathy. , 1989, Metabolism: clinical and experimental.

[114]  M L Wolbarsht,et al.  Lasers in ophthalmology: the path from theory to application. , 1979, Applied optics.

[115]  U. Malmqvist,et al.  Stretch-dependent modulation of contractility and growth in smooth muscle of rat portal vein. , 2000, Circulation research.

[116]  M. Derwahl,et al.  Increased levels of platelet-derived growth factor in vitreous fluid of patients with proliferative diabetic retinopathy. , 2000, Experimental and clinical endocrinology & diabetes : official journal, German Society of Endocrinology [and] German Diabetes Association.

[117]  M. Doğru,et al.  Modifying factors related to asymmetric diabetic retinopathy , 1998, Eye.

[118]  Bruce A. Berkowitz,et al.  A comparative study of the effects of argon and diode laser photocoagulation on retinal oxygenation , 1997, Graefe's Archive for Clinical and Experimental Ophthalmology.

[119]  J. W. Mcmeel,et al.  Regional retinal blood flow reduction following half fundus photocoagulation treatment. , 1994, The British journal of ophthalmology.

[120]  R. Simó,et al.  Vitreous levels of vascular endothelial growth factor are not influenced by its serum concentrations in diabetic retinopathy , 1997, Diabetologia.

[121]  H. Shimada,et al.  Vitrectomy for diabetic cystoid macular edema. , 2001, Japanese journal of ophthalmology.

[122]  C. H. Chen,et al.  Evidence of the presence of a specific vascular endothelial growth factor in fetal bovine retina. , 1987, Experimental cell research.

[123]  R. Banerjee,et al.  Artificial vitreous replacements. , 2003, Bio-medical materials and engineering.

[124]  Ali Erginay,et al.  Optical coherence tomography for evaluating diabetic macular edema before and after vitrectomy. , 2003, American journal of ophthalmology.

[125]  M. Blumenkranz,et al.  Vitrectomy for diabetic macular traction and edema associated with posterior hyaloidal traction. , 1992, Ophthalmology.

[126]  F. Fankhauser,et al.  Clinical studies on high and low power laser radiation upon some structures of the anterior and posterior segments of the eye , 1982, International Ophthalmology.

[127]  E. Stefánsson,et al.  Oxygenation and vasodilatation in relation to diabetic and other proliferative retinopathies. , 1983, Ophthalmic surgery.

[128]  S L Jacques,et al.  Melanin granule model for laser-induced thermal damage in the retina , 1996, Bulletin of mathematical biology.

[129]  B. Petrig,et al.  Effect of panretinal photocoagulation on retinal blood flow in proliferative diabetic retinopathy. , 1986, Ophthalmology.

[130]  A. Ooshima,et al.  Stretch-induced proliferation of cultured vascular smooth muscle cells and a possible involvement of local renin-angiotensin system and platelet-derived growth factor (PDGF). , 1997, Hypertension research : official journal of the Japanese Society of Hypertension.

[131]  K. Nakagawa,et al.  Hypoxia-induced expression of vascular endothelial growth factor by retinal glial cells promotes in vitro angiogenesis , 1995, Virchows Archiv.

[132]  P. Campochiaro,et al.  Pigment epithelium‐derived factor inhibits retinal and choroidal neovascularization , 2001, Journal of cellular physiology.

[133]  D. S. Mcleod,et al.  Retinal vascular development and oxygen-induced retinopathy: a role for adenosine , 2003, Progress in Retinal and Eye Research.

[134]  Joan W. Miller,et al.  Systemic hyperoxia decreases vascular endothelial growth factor gene expression in ischemic primate retina. , 1997, Archives of ophthalmology.

[135]  E. Stefánsson,et al.  Vitrectomy prevents retinal hypoxia in branch retinal vein occlusion. , 1990, Investigative ophthalmology & visual science.

[136]  C. Kahn,et al.  Receptors and growth-promoting effects of insulin and insulinlike growth factors on cells from bovine retinal capillaries and aorta. , 1985, The Journal of clinical investigation.

[137]  M L Wolbarsht,et al.  The corneal contact lens and aqueous humor hypoxia in cats. , 1983, Investigative ophthalmology & visual science.

[138]  K. Diddie,et al.  The effect of photocoagulation on the choroidal vasculature and retinal oxygen tension. , 1977, American journal of ophthalmology.

[139]  R. Danis,et al.  Hyperoxia improves contrast sensitivity in early diabetic retinopathy. , 1996, The British journal of ophthalmology.

[140]  M L Wolbarsht,et al.  The rationale of photocoagulation therapy for proliferative diabetic retinopathy: a review and a model. , 1980, Ophthalmic surgery.

[141]  N. Tachi,et al.  Vitrectomy for diffuse macular edema in cases of diabetic retinopathy. , 1996, American journal of ophthalmology.

[142]  Ying-Bo Shui,et al.  Vitrectomy surgery increases oxygen exposure to the lens: a possible mechanism for nuclear cataract formation. , 2005, American journal of ophthalmology.

[143]  Einar Stefansson,et al.  Oxygen and diabetic eye disease , 2004, Graefe's Archive for Clinical and Experimental Ophthalmology.

[144]  E. Stefánsson,et al.  The effect of photocoagulation on the oxygenation and ultrastructure of avascular retina. , 1990, Experimental eye research.

[145]  Joan W. Miller,et al.  Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model. , 1994, The American journal of pathology.

[146]  M. Tso,et al.  Experimental photocoagulation of the human retina. I. Correlation of physical, clinical, and pathologic data. , 1977, Archives of ophthalmology.

[147]  Joan W. Miller,et al.  Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. , 1994, American journal of ophthalmology.

[148]  Schmidt Re,et al.  Histopathology of retinal lesions produced by long-term laser exposure. , 1977 .

[149]  L'esperance Fa,et al.  An opthalmic argon laser photocoagulation system: design, construction, and laboratory investigations. , 1968 .

[150]  E. Stefánsson,et al.  Laser treatment and the mechanism of edema reduction in branch retinal vein occlusion. , 2000, Investigative ophthalmology & visual science.

[151]  G. Green,et al.  Laser Doppler measurements of the effect of panretinal photocoagulation on retinal blood flow. , 1982, Ophthalmology.

[152]  A. Ljubimov,et al.  Basement membrane and growth factor gene expression in normal and diabetic human retinas. , 1999, Current eye research.

[153]  L. Cantley,et al.  HGF-mediated chemotaxis and tubulogenesis require activation of the phosphatidylinositol 3-kinase. , 1995, The American journal of physiology.

[154]  G F Vrensen,et al.  Endothelial cell hypertrophy induced by vascular endothelial growth factor in the retina: new insights into the pathogenesis of capillary nonperfusion. , 2001, Archives of ophthalmology.

[155]  M. Matsumoto,et al.  Hypoxia-mediated induction of acidic/basic fibroblast growth factor and platelet-derived growth factor in mononuclear phagocytes stimulates growth of hypoxic endothelial cells. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[156]  Toke Bek,et al.  Visual prognosis after panretinal photocoagulation for proliferative diabetic retinopathy. , 2005, Acta ophthalmologica Scandinavica.

[157]  P. Campochiaro,et al.  Basic fibroblast growth factor is neither necessary nor sufficient for the development of retinal neovascularization. , 1998, The American journal of pathology.

[158]  M. Boulton,et al.  The pathogenesis of diabetic retinopathy: old concepts and new questions , 2002, Eye.

[159]  H. Yamashita,et al.  Early postoperative retinal thickness changes and complications after vitrectomy for diabetic macular edema. , 2003, American journal of ophthalmology.

[160]  J. Mellerio,et al.  Histology of the formation of retinal laser lesions. , 1967, Experimental eye research.

[161]  G. Blankenship,et al.  Long-term diabetic vitrectomy results. Report of 10 year follow-up. , 1985, Ophthalmology.