Intraretinal oxygen distribution and consumption during retinal artery occlusion and graded hyperoxic ventilation in the rat.

PURPOSE To determine intraretinal oxygen distribution and consumption in a rat model of retinal artery occlusion during air breathing and stepwise systemic hyperoxia. METHODS Laser occlusion of the pair of retinal arteries feeding the area of retina under investigation was performed. Oxygen-sensitive microelectrodes were then used to measure oxygen tension as a function of depth through the retina. Breathing mixtures were manipulated to produce stepwise increments in systemic oxygen levels, and the measurement of intraretinal oxygen distribution was repeated. Oxygen distribution in the retina was analyzed by an established eight-layer mathematical model of retinal oxygen consumption. RESULTS Intraretinal oxygen distribution in the occluded area confirmed that the choroid was the only source of retinal oxygenation. Under air-breathing conditions, the oxygen supply from the choroid was sufficient to support the photoreceptor inner segments. Any remaining oxygen was consumed by the outer plexiform layer. Increases in inspired oxygen level reduced the extent of inner retinal anoxia. However, some degree of anoxia in the innermost retina was usually present. CONCLUSIONS Occlusion of the retinal circulation renders most of the inner retina anoxic. Ventilation with 100% oxygen does not generally avoid some degree of intraretinal anoxia. With 100% oxygen ventilation, the oxygen consumption of the inner retina was more than four times that of the outer retina. A marked degree of heterogeneity in oxygen uptake of different retinal layers was evident. The dominant oxygen consumers were the inner segments of the photoreceptors, the outer plexiform layer, and the inner plexiform layer.

[1]  Dao-Yi Yu,et al.  Intraretinal oxygenation and oxygen consumption in the rabbit during systemic hyperoxia. , 2004, Investigative ophthalmology & visual science.

[2]  S. Cringle,et al.  PO2 profiles and oxygen consumption in cat retina with an occluded retinal circulation. , 1990, Investigative ophthalmology & visual science.

[3]  R. Hawkins,et al.  Cerebral Energy Metabolism , 1985 .

[4]  S. Cringle,et al.  Light-induced changes in retinal oxygen consumption. , 1996, Investigative ophthalmology & visual science.

[5]  M. Sanders Vision and Circulation , 1977 .

[6]  M. Landers Retinal oxygenation via the choroidal circulation. , 1978, Transactions of the American Ophthalmological Society.

[7]  Dao-Yi Yu,et al.  Outer retinal anoxia during dark adaptation is not a general property of mammalian retinas. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[8]  J. Dickinson,et al.  Retinopathy of prematurity: recent advances in our understanding , 2002, Archives of disease in childhood. Fetal and neonatal edition.

[9]  S. Cringle,et al.  Light and choroidal PO2 modulation of intraretinal oxygen levels in an avascular retina. , 1999, Investigative ophthalmology & visual science.

[10]  D. Fox,et al.  Oxygen consumption in the rat outer and inner retina: light- and pharmacologically-induced inhibition. , 1995, Experimental eye research.

[11]  P. Nair,et al.  A microelectrode for measuring intracellular PO2. , 1967, Journal of applied physiology.

[12]  Dao-Yi Yu,et al.  A multi-layer model of retinal oxygen supply and consumption helps explain the muted rise in inner retinal PO(2) during systemic hyperoxia. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[13]  T. K. Goldstick,et al.  Retinal oxygen tension and oxygen reactivity in retinopathy of prematurity in kittens. , 1984, Investigative ophthalmology & visual science.

[14]  S. Cringle,et al.  Intraretinal oxygen distribution in the rat with graded systemic hyperoxia and hypercapnia. , 1999, Investigative ophthalmology & visual science.

[15]  Dao-Yi Yu,et al.  Oxygen consumption in the avascular guinea pig retina. , 1996, The American journal of physiology.

[16]  C. Pournaras,et al.  Experimental retinal vein occlusion: effect of acetazolamide and carbogen (95% O2/5% CO2) on preretinal PO2. , 2004, Investigative ophthalmology & visual science.

[17]  H. Saltzman,et al.  RETINAL OXYGEN UTILIZATION MEASURED BY HYPERBARIC BLACKOUT. , 1964, Archives of ophthalmology.

[18]  Robert A. Linsenmeier,et al.  Oxygen distribution in the macaque retina. , 1993, Investigative ophthalmology & visual science.

[19]  Dao-Yi Yu,et al.  Oxygen Distribution and Consumption within the Retina in Vascularised and Avascular Retinas and in Animal Models of Retinal Disease , 2001, Progress in Retinal and Eye Research.

[20]  C. Pournaras,et al.  Diffusion of O2 in normal and ischemic retinas of anesthetized miniature pigs in normoxia and hyperoxia , 2004, Graefe's Archive for Clinical and Experimental Ophthalmology.

[21]  S. Cringle,et al.  Vitreal and retinal oxygenation , 2004, Graefe's Archive for Clinical and Experimental Ophthalmology.

[22]  K Mervin,et al.  Limiting photoreceptor death and deconstruction during experimental retinal detachment: the value of oxygen supplementation. , 1999, American journal of ophthalmology.

[23]  D. McCandless Cerebral Energy Metabolism and Metabolic Encephalopathy , 1985, Springer US.

[24]  E. Stefánsson,et al.  In vivo O2 consumption in rhesus monkeys in light and dark. , 1983, Experimental eye research.

[25]  H. W. Reading,et al.  The metabolism of the dystrophic retina—I: Comparative studies on the glucose metabolism of the developing rat retina, normal and dystrophic , 1962 .

[26]  T K Goldstick,et al.  Oxygen consumption in the inner and outer retina of the cat. , 1995, Investigative ophthalmology & visual science.

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

[28]  Dao-Yi Yu,et al.  Oxygen distribution and consumption in the developing rat retina. , 2006, Investigative ophthalmology & visual science.

[29]  R. Linsenmeier,et al.  Effects of light and darkness on oxygen distribution and consumption in the cat retina , 1986, The Journal of general physiology.

[30]  Eng H. Lo,et al.  Neurological diseases: Mechanisms, challenges and opportunities in stroke , 2003, Nature Reviews Neuroscience.

[31]  Landers Mb rd Retinal oxygenation via the choroidal circulation. , 1978 .

[32]  P. Nair,et al.  A microelectrode for measuring intracellular pH. , 1967, Advances in experimental medicine and biology.

[33]  I J Constable,et al.  Robotic ocular ultramicrosurgery. , 1998, Australian and New Zealand journal of ophthalmology.

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

[35]  Dao-Yi Yu,et al.  Low oxygen consumption in the inner retina of the visual streak of the rabbit. , 2004, American journal of physiology. Heart and circulatory physiology.

[36]  S. Cringle,et al.  Modelling oxygen consumption across an avascular retina. , 1996, Australian and New Zealand journal of ophthalmology.

[37]  Dao-Yi Yu,et al.  Intraretinal oxygen distribution in rats as a function of systemic blood pressure. , 1994, The American journal of physiology.

[38]  Dao-Yi Yu,et al.  Intraretinal oxygen distribution in the monkey retina and the response to systemic hyperoxia. , 2005, Investigative ophthalmology & visual science.

[39]  Dao-Yi Yu,et al.  Intraretinal oxygen consumption in the rat in vivo. , 2002, Investigative ophthalmology & visual science.

[40]  Dao-Yi Yu,et al.  Oxygen distribution in the mouse retina. , 2006, Investigative ophthalmology & visual science.