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Fundus Autoflourescence

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Fundus Autoflourescence; The retinal pigment epithelium - photoreceptor complex, and macular pigment.

Dirk J Booysen

Dip Optom FOA (SA), MC Optom (UK), TMOD (USA), CAS (USA)

December 2010

Fundus autofluorescence using a confocal scanning laser ophthalmoscope (cSLO) was first described by Von Rückmann A, Fitzke, et al. in 1995.46 The cSLO was used to image the distribution of lipofuscin in the retinal pigment epithelium in vivo. Autofluorescence was shown to be abnormally high in certain inherited diseases and low in the presence of retinal atrophy. At the same time during 1995 Delori FC, Dorey CK, et al.13 used a fundus spectrophorometer to measure the autofluorescence in vivo at the fovea and 7o temporal to the fovea. They concluded that spectral characteristics, correlation with age, topographic distribution and retinal location between the choriocapilaris and photoreceptors strongly suggest that fundus autofluorescence arises primarily from lipofuscin in the retinal pigment epithelium. Autofluorescence photography of the retina therefore provides important diagnostic information about diseases that affect the outer retina; more specifically the retinal pigment epithelium and photoreceptors. (Schmitz-Valckenberg S, Holz F. April 2008)32. It can also be used to evaluate macular pigment density (Delori F C, Goger D G, et al. 2001)11, and other diseases of the retina and choroid. It is a non invasive clinical tool which has the potential to revolutionarise clinical retina practice. Before discussing the technology it is important to understand the role of the outer retina (retinal pigment epithelium - photoreceptor complex) and the macular pigment in fundus autofluorescence.

The retinal pigment epithelium.

The retinal pigment epithelium is a monolayer of cells, cuboidal in cross section and hexagonal viewed from above. The zonula occludens bind the cells together forming the equivalent of the blood retinal barrier formed by the capillary endothelium of the retinal vasculature. The cells are roughly 10 - 14 microns in size at the fovea but they become flatter and broader peripherally (60 microns in size). Overlying each retinal pigment epithelial cell are about 45 photoreceptor cells for which it is metabolically responsible (Hogan M J, Alvarado J A, Weddell J E. 1971)20. The apical side facing the photoreceptors have long microvilli that reach up between and envelop the outer segments of the photoreceptors. Melanin pigment granules are concentrated in the apical end of the cells while the mid portion contains the nucleus, Golgi apparatus, endoplasmic recticulum, and digestive vesicles. The basal membrane has convoluted infolds to increase the surface area for the absorption and secretion of material. The retinal pigment epithelium actively engage in oxidative metabolism, enzymes are synthesised for functions such as membrane transport, visual pigment metabolism, digestion of waste products as well as limiting the formation of free radicals which damage the lipid membranes. The retinal pigment epithelium also contributes to the function and maintenance of the inter receptor matrix, critical to retinal adhesion. It is part of a complex system of cellular cross talk that controls vascular supply, permeability, growth and repair as well as other processes vital to retinal function (Marmor M F. 1999)25. The melanin pigment is present within cytoplasmic granules called melanosomes and is responsible for the absorption of stray light minimising light scatter. It also serves as a free radical stabilizer and can bind with toxins as well as retinotoxic drugs such as chloroquine and thioridazine. Another pigment present in the retinal pigment epithelium is lipofuscin which accumulates gradually with age until the cells are severely clogged with the golden autofluorescent pigment with up to 19% of the cytoplasmic volume containing lipofuscin by the age of 80 years. The lipofuscin granules accumulate predominantly in the peripheral cell margin while the absorbing melanin granules are oriented toward the apical cell centre and the cell nucleus is located at the basal cell side. Figure 1. Retinal pigment epithelium cells also produce lipofuscin rich deposits that may accumulate as drusen within Bruch's membrane. As they enlarge drusen become the earliest lesions in age related macular degeneration (Whitehead A J, Mares J A, Danis R P. 2006)48. Photoreceptors and retinal pigment epithelium are continually exposed to light and oxygen which facilitate the production of free radicals that can damage membranes over time. The retinal pigment epithelium is responsible for cellular renewal by phagocytosis of the photoreceptor outer segment discs and synthesis of new discs (Young R W. 1976)50. The phagocytosed discs become encapsulated in vesicles within the retinal pigment epithelial cells (phagosomes), which merge with lysosymes which digest the material. Fatty acids are retained and waste products are excreted across the basal retinal pigment epithelial membrane. Over time residual debris contribute to the formation of lipofuscin. These fluorophores are unusual and not amenable to degradation by lysosymes leading to the accumulation of lipofuscin in the retinal pigment epithelial cells (Sparrow J R, Boulton M. 2005)39. It is not clear if lipofuscin damages retinal pigment epithelial cells or is simply a marker for cellular damage but excessive accumulation of retinal pigment epithelial lipofuscin in autosomal - recessive Stargardt macular degeneration is considered to be the cause of retinal pigment epithelium atrophy.

Macular pigment.

The macular pigment consists of two carotenoids lutein and zeaxanthin. Lutein is structurally related to α-carotene and zeaxanthin to β-carotene, however they are not provitamin A carotenoids. Lutein and Zeaxanthin are especially concentrated in leafy green vegetables, many fruits and coloured vegetables such as squash, sweet peppers, sweet corn, and peas. In primates carotenoids cannot be synthesised de novo and have to be taken in by nutrition. The retina has the highest concentration of xanthophylls of any tissue, almost exclusively lutein and zeaxanthin, with the highest concentration in the centre of the fovea. Zeaxanthin is the leading carotenoid in this location, declining with increasing eccentricity in favour of lutein (Whitehead A J, Mares J A, Danis R P. 2006)48. The highest carotenoid concentration is in the pre-receptor axon layer of the fovea and extrafoveal macula. Macular pigment's absorbance spectrum peaks at 460nm, preventing damaging light to reach the photoreceptors (and retinal pigment epithelium cells) in the fovea.

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