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Analysis of the Macular Pigment by HPLG Retinal Distribution and Age Study

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Analysis of the Macular Pigment by HPLG Retinal Distribution and Age Study Investigative Ophthalmology & Visual Science, Vol. 29, No. 6, June 1988 Copyright © Association for Research in Vision and Ophthalmology Analysis of the Macular Pigment by HPLG Retinal Distribution and Age Study Richard A. Done,* John T. Landrum.t Lilio Fernandez, f and Sara L. Tarsis* High performance liquid chromatography (HPCL) has been employed to study the distribution throughout the human retina of zeaxanthin and lutein, the two major components of the macular pigment. Differences between individuals have also been studied with a view to uncovering possible age-related effects. Both pigments were detected in prenatal eyes (~20 weeks gestation) but did not form a visible yellow spot. Generally they were not easily discernible until about 6 months after birth. For 87 donors between the ages of 3 and 95, no dependence on age was observed in the quantity of either pigment. For ~90% of these, zeaxanthin was dominant. For the remaining 10%, as well as for the seven youngest donors, all below the age of 2, and in prenatal eyes, lutein was the major pigment. In individual retinas, the lutein:zeaxanthin ratio increased from an average of approximately 1:2.4 in the central 0-0.25 mm to over 2:1 in the periphery (8.7-12.2 mm). The variation in this ratio with eccentricity was linearly correlated with the corresponding rodxone ratio. A selective mechanism of uptake, which results in cones and rods preferentially acquiring zeaxanthin and lutein, respectively, could explain this correlation. Invest Ophthalmol Vis Sci 29:843-849, 1988 The role of the macular pigments may be two-fold: has been addressed in a number of psychophysical to improve visual acuity1 and to protect retinal tissue investigations.8"11 One such study,9 involving sub- against photodegradation.2 While feeding studies jects in the age range 10 to 90, uncovered wide varia- using monkeys demonstrate the dietary origin of the tions in the optical density of their pigment, but no macular pigments,3 there are no reports on the mech- significant dependence on age. Optical densities ob- anism of their uptake by the neural retina. Is the tained by psychophysical methods, such as sensitivity mechanism highly discriminating, or are the pig- measurements," however, rest upon the validity of a ments transported nonselectively into retinal cells? number of assumptions. (See Pease et al10 for review Our recent observations, that the isomeric dihy- as well as means of circumvention.) Chemical analy- droxy-carotenoids, zeaxanthin and lutein, constitute sis, on the other hand, is relatively straightforward the macular pigment,4 might favor the latter. Alterna- and, being independent of observer skill, may be used tively, a selective uptake mechanism might deliver equally reliably on all age groups, including prenatal. the two pigments to different target cells within the retina. To explore these possibilities, we have applied high performance liquid chromatography (HPLC) to Materials and Methods examine the variation in pigment density and com- position with retinal location and age. The rationale Sample Preparation for this approach was that the dependence of the cell populations on retinal eccentricity5 and age6'7 might Frozen donor eyes were provided by the Florida be reflected in the macular pigments. Lions Eye Bank and the National Disease Research The variability in pigmentation among individ- Interchange, and were stored in sealed containers at uals, including the possible contributing factor of age, -100°C until needed. Fetal eyes, supplied through the latter organization, were shipped on ice and ana- lyzed immediately. Dissection of the thawed eye was From the Departments of *Physics and fChemistry, Florida In- ternational University (The State University of Florida at Miami), performed in 0.9% saline solution. After the neural Miami, Florida. retina had been separated, it was trimmed by cutting Presented in part at the 1986 and 1987 meetings of ARVO, around the equator, and inspected for signs of dam- Sarasota, Florida. age such as holes, tears or separation of retinal layers. Supported by NIH/MBRS Grant RR-O82O5-O2A3. If such damage occurred in the retinal area intended Submitted for publication: June 30, 1987; accepted December 7, for analysis, the macula was put aside for future use. 1987. Reprint requests: Richard A. Bone, PhD, Department of Physics, About 40% of all retinas were found to be unsuitable Florida International University, Miami, FL 33199. for the present study. 843 Downloaded from iovs.arvojournals.org on 10/02/2021 844 INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / June 1988 Vol. 29 l_Microscope was employed, this being sufficiently large to include the largest macula lutea. By placing the retina on a spherical surface, selected to match as closely as pos- sible the curvature of the retina, problems of tears, folds or stretching were virtually eliminated. For the very small prenatal eyes, however, this technique was not feasible. Instead, extracts from the entire neural retina were analyzed for the presence of carotenoids. Each annulus or disk of retinal tissue was trans- ferred to a glass tissue homogenizer, to which was added a known mass (~ 10 ng) of lutein monomethyl ether, as an internal standard, and about 2 to 3 ml of acetone for extraction of the carotenoids. This ether is readily prepared from lutein,12 and its HPLC reten- tion time corresponds to a window in the retinal chromatogram. Furthermore, its similarity of struc- ture to lutein and zeaxanthin should render it equally sensitive to decomposition during work-up and chro- matography (see Results). The acetone solutions were centrifuged at low speed, filtered (0.2 nm nylon-mesh syringe-filters), and dried in 5 ml pear-drop flasks under a stream of pure nitrogen. With extracts from larger tissue samples, greasy contaminants were Fig. 1. Apparatus used for dissecting retinas into annuli concen- clearly visible on the walls of the flask. It was possible tric with the fovea. to preferentially dissolve the carotenoids by briefly swirling cold (-20°C) acetone around the prechilled flask and quickly transferring it to a clean flask where A lucite sphere, approximately matching the cur- it was dried prior to injection on the HPLC. vature of the retina (1 inch diameter for adults), was placed in the saline-filled dissecting dish, and the ret- Quantification by HPLC ina maneuvered into position above it. Upon lifting the sphere from the solution, the retina could be HPLC was conducted on an LDC/Milton Roy sys- placed smoothly over it without folds or wrinkles. tem (LDC/Milton Roy, Riviera Beach, FL) including The sphere, with the retina uppermost, was then a Spectromonitor D UV-visible detector (0-0.001 seated in a rubber-lined ring in the apparatus shown absorbance units full-scale) set at 450 nm. At this in Figure 1. wavelength, absorption by zeaxanthin is maximum; that of lutein is ~92% of maximum. A 250 X 4.6 mm Co-axial with the ring was a low-power microscope column with C18 reversed-phase support (5 nm with cross-wires on which the operator centered the Spherisorb ODS1) was supplied by Keystone Scien- fovea by rotation of the sphere. In order to analyze tific (State College, PA). Essentially baseline separa- the distribution of macular pigments as a function of tion was achieved isocratically with an eluent com- retinal eccentricity, the microscope tube was replaced posed of 92% methanol and 8% water/acetonitrile in the upper aluminum block (Fig. 1) by a set of (3:1 v/v) and a flow rate of 1 ml min~'. spaced, concentric, tubular cutters, designed to slide telescopically relative to one another and to the upper block itself. By bearing down with these onto the Results sphere, the retina could be cut into six annuli, con- Age Study centric with the fovea. Only adult eyes were used for this part of the study. The ranges of linear surface A typical chromatogram, labeled a), representing distance, from the center of the fovea to the inner and the pigments found in the central portion of the ret- outer edges of the annuli, were 0-0.75, 0.75-1.6, ina (0-2.3 mm), is shown in Figure 2. The dominant 1.6-2.5, 2.5-5.8, 5.8-8.7, and 8.7-12.2 mm. A single zeaxanthin peak and the secondary lutein peak were cutter, 0-0.25 mm, was also available, but could not found in the great majority of samples analyzed, with be used in conjunction with this set. For the age the reversed situation occurring only rarely. The four study, a single cutter covering the range 0-2.3 mm minor peaks have not yet been identified; however, Downloaded from iovs.arvojournals.org on 10/02/2021 No. 6 MACULAR PIGMENT: RETINAL DISTRIBUTION AND AGE STUDY / Done er ol. 845 Fig. 2. Representative chromatograms of pigments extracted from retinal tis- sue. L = lutein, Z = zeax- anthin, detector wavelength = 450 nm. Chromatogram a), for a 47-year-old donor, was obtained from a central disk (0-2.3 mm), as used in the age study. Chromato- grams b), c), and d), for a 65-year-old donor, illustrate 2.5-5.8mm the dramatic change in the lutein:zeaxanthin ratio with retinal eccentricity. For the 1.6-2.5 mm | Retinal sake of clarity, the internal distribution standard peak (retention study time ~24 min), has been omitted. 0 - 2.3 mm A Age study 10 20 30 Time, minutes their spectra indicate that they too are carotenoids masses of zeaxanthin and lutein varied considerably and it is conceivable that they are cis-trans isomers of among donors, as illustrated by the frequency distri- lutein or zeaxanthin.13 Their presence raises the ques- bution of Figure 3, neither this nor the composition tion of which pigments constitute the macular pig- of the pigment showed any significant variation with ment.
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