IOVS Annual Reviews: Physical Science Suite
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
 QUICK SEARCH:   [advanced]


     


(Investigative Ophthalmology and Visual Science. 2007;48:3783-3787.)
© 2007 by The Association for Research in Vision and Ophthalmology, Inc.
DOI:  10.1167/iovs.06-1218

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (3)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Wolf-Schnurrbusch, U. E. K.
Right arrow Articles by Wolf, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Wolf-Schnurrbusch, U. E. K.
Right arrow Articles by Wolf, S.

Ethnic Differences in Macular Pigment Density and Distribution

Ute E. K. Wolf-Schnurrbusch,1 Nicole Röösli,1 Eva Weyermann,1 Mirjam R. Heldner,1 Katja Höhne,2 and Sebastian Wolf1

1From the Klinik und Poliklinik für Augenheilkunde, Inselspital, University Bern, Bern, Switzerland; and the 2Augenklinik der Charité, Universitätsmedizin Berlin, Berlin, Germany.


    Abstract
 Top
 Abstract
 Materials and Methods
 Results
 Discussion
 References
 
PURPOSE. Many epidemiologic studies suggest a number of risk factors that may be associated with progression of age-related maculopathy (ARM). In this study, the authors investigate ethnic differences in macular pigment density (MPD) and macular pigment (MP) distribution.

METHODS. Inclusion criteria were healthy subjects, aged 35 to 49 years, visual acuity ≥20/20, race ethnicity white non-Hispanic (WNH) or African. All subjects underwent the following examinations: best-corrected ETDRS visual acuity (VA), measurements of MPD, and spatial distribution of MP with a modified confocal scanning laser ophthalmoscope according to a standard protocol. MPD maps were calculated from autofluorescence images recorded at 488 nm and 514 nm. Central macular pigment density (MPDc) was quantified from MPD maps within 0.5° around the center of the fovea.

RESULTS. In total, 118 healthy subjects (61 women, 57 men) aged 35 to 49 years (mean, 42.5 ± 3.6 years) were recruited for the study. Sixty-seven healthy subjects were WNH and 51 were African. Visual acuity ranged from 20/20 to 20/16 in the study eye. Significant differences were found among MPDc between the group of WNH (MPDc, 0.36 ± 0.13 density units [DU]; P < 0.0001) and African subjects (MPDc, 0.59 ± 0.14 DU). A parafoveal ring was significantly more frequent in African subjects than in WNH subjects (86% [African] vs. 68% [WNH]; P < 0.0001).

CONCLUSIONS. This study demonstrates that ethnicity plays a role in MPD values and in MP distribution. The association of different distribution patterns and their relevance as possible prognostic factors for diseases leading to oxidative retinal damage requires further studies.


The pathogenesis of age-related macular degeneration (ARMD) remains putative. It is assumed to be a multifactorial disease leading to oxidative retinal damage.1 2 3 4 5 It is classified as the end stage of age-related maculopathy (ARM), which is characterized by degenerative disorder of the central area of the retina.6 Recent studies report that the incidence of ARMD strongly depends on the age of the person and the stage of ARM.7 8 Many epidemiologic studies suggest a number of risk factors that may be associated with progression of ARM. These include personal characteristics such as race and ocular characteristics such as iris pigmentation and macular pigment density (MPD).9 10 11

Highly significant risk factors, such as genetic variants of complement factors H and B, which occur in more than 50% of all patients with ARMD were recently observed.12 13 Most observers agree that ARMD is more common in white persons than in persons of African race.14 Congdon et al.11 reported in 2004 that the leading cause of blindness among white persons older than 40 in the United States is ARMD (54.4%), whereas among African persons it is 4.4%, indicating the possibility that protective genetic variants may exist in African persons. Previously, we showed15 that central macular pigment density (MPDc) is similar in patients with ARM and healthy controls, but we found a large variation in macular pigment (MP) distribution.

By analyzing autofluorescence images, Delori et al.16 found a variation in the spatial distribution of MP from a single central peak that decreased monotonically with increasing eccentricity to a bimodal distribution with a central peak surrounded by a ring with high-density values of MP. Berendschot et al.17 confirmed and strengthened their results after adding the technique of reflectance spectroscopy.

In this study, we investigated the ethnic differences of different patterns of MP distribution and their relation to MPDc in healthy subjects of various ethnic phenotypes. Most current studies about MP are mainly derived from white non-Hispanic (WNH) subjects, and only a few are derived from Asian subjects.18 19


    Materials and Methods
 Top
 Abstract
 Materials and Methods
 Results
 Discussion
 References
 
We included healthy subjects between 35 and 49 years of age with a race ethnicity of WNH or African. The research followed the tenets of the Declaration of Helsinki. Informed consent was obtained from each subject after explanation of the nature and possible risks of our study. Institutional Review Board approval was granted. In total we recruited 118 healthy subjects (61 women, 57 men) from 35 to 49 years of age (mean, 43 ± 4 years) for the study. Sixty-seven healthy subjects were WNH (35 women, 32 men) and 51 were African (26 women, 25 men). Visual acuity ranged from 20/20 to 20/16 in the study eye. Neither distribution of additional ARMD risk factors (e.g., gender, family history, status of smoking) nor mean age distribution differed between the groups (mean ageWNH: 43.0 ± 3.8 years vs. mean ageAfrican: 41.8 ± 3.3 years).

One eye of each subject was randomly selected and included in the study. All subjects underwent comprehensive ocular examination. The pupil of the study eye was dilated with eye drops containing 0.5% tropicamide and 2.5% phenylephrine. Macular pigment measurements were obtained with the modified confocal scanning laser ophthalmoscope (mpHRA; Heidelberg Engineering, Heidelberg, Germany)20 using autofluorescence images obtained at two wavelengths based on the pioneering work of Delori et al.21 Subjects were positioned in front of the tabletop and instructed to look straight ahead and to remain steady. We then obtained 20° autofluorescence images at excitation wavelengths of 488 nm and 514 nm of the posterior pole, with a high-pass filter transmitting at a wavelength greater than 530 nm.

As reported previously,22 we quantified macular pigment densities by calculating a MPD map and comparing foveal and parafoveal autofluorescence at 488 nm and 514 nm (Fig. 1) . Density maps were processed to calculate MPDc within a 1°-diameter circle centered on the fovea. MPDc is expressed in optical density units (DU). All quantitative analyses were performed by the software provided by the manufacturer of the scanning laser ophthalmoscope.


Figure 1
View larger version (31K):
[in this window]
[in a new window]

 
FIGURE 1. Modified confocal scanning laser ophthalmoscope (a). Autofluorescence images at 488 nm (b) and 514 nm (c). Wavelengths, absorbance spectrum of MP (d). Formula for calculation of MPD map (e). Three-dimensional image of spatial distribution of MP (f).

 
In addition to the value of MPDc, we looked at the spatial distribution of MP. We assumed that the spatial distribution of MP is circularly symmetric around the fovea. Therefore, we calculated radial density profiles by calculating the mean MPD for each radius around the fovea. The mean MPD for each eccentricity was calculated by dividing the sum of all optical densities at a given radius by the number of pixels making up a circle at a given radius. These values were plotted against the distance to the fovea and were graphically displayed (Fig. 2) . Density profiles were analyzed for the presence of a parafoveal ring and for the location of the maximum of this parafoveal ring. A parafoveal ring was assumed to be present if the density profile could not be approximated by a monotonic decay function and a shoulder could be identified within 3° from the peak density. Because width at half maximum is a key descriptor of distribution, we analyzed our profiles looking for the width of the spatial macular pigment distribution. All profiles were examined by two independent observers. In the event of a discrepancy between the two observers, the differences were discussed and a third observer was asked for the final decision. Additionally, we calculated the mean MPD (MPD05–1) within the interval between 0.5° and 1° radius around the fovea. We calculated the ratio MPD05–1/MPDc to characterize the significance of the parafoveal ring.


Figure 2
View larger version (59K):
[in this window]
[in a new window]

 
FIGURE 2. Screen shot of MP maps and distribution profiles. (a) Typical MP distribution with a central peak (MPD05–1/MPDc = 0.50). (b) MP distribution with a parafoveal ring (MPD05–1/MPDc = 0.74).

 
Mean value and SD are given for all samples with normal distributions (Kolmogorov-Smirnov test) and for abnormal distributions, medians, and percentiles (2.5% and 97%). The Mann-Whitney U test was used to assess the significance of the differences between the groups. Findings with an error probability of < 0.05 were considered statistically significant; {chi}2 analysis was used to determine the differences in frequency of the presence of a parafoveal ring among the different groups.


    Results
 Top
 Abstract
 Materials and Methods
 Results
 Discussion
 References
 
Significant differences were found among MPDc between the groups of WNH and African subjects (0.36 ± 0.13 DU vs. 0.59 ± 0.14 DU; P < 0.01; Fig. 3 ). The parafoveal ring was significantly more frequent in African subjects than in WNH subjects (44 of 51, 86% [African] vs. 46 of 67, 68% [WNH]; P < 0.01). The maximum of this parafoveal ring was found at 0.66° ± 0.13° (range, 0.48°-1.2°) from the fovea. The maximum of the ring was located at a mean of 0.67° ± 0.13° in the African subjects and at a mean of 0.64° ± 0.10° in WNH subjects. Width at half maximum, as a key descriptor of distribution, was significantly larger in African subjects than in WNH subjects (0.91° ± 0.23° vs. 0.75° ± 0.15°; P < 0.05).


Figure 3
View larger version (11K):
[in this window]
[in a new window]

 
FIGURE 3. Box plot for MPDc in DU. Data for WNH and African subjects.

 
Significant differences were found among the ratio MPD05–1/MPDc between the groups of WNH and African subjects (0.77 ± 0.12 vs. 0.85 ± 0.09; P < 0.01; Fig. 4 ). The mean ratio MPD05–1/MPDc was 0.86 ± 0.07 for subjects with a visible parafoveal ring compared with 0.71 ± 0.42 for subjects with a peak (P < 0.001). We could not detect any statistically significant effect of additional factors, such as family history of ARMD, smoking status, or iris color.


Figure 4
View larger version (11K):
[in this window]
[in a new window]

 
FIGURE 4. Box plot for ratio MPD05–1/MPDc. Data for WNH and African subjects.

 

    Discussion
 Top
 Abstract
 Materials and Methods
 Results
 Discussion
 References
 
Various epidemiologic studies have focused on the analysis of risk factors for the development of ARM and ARMD.23 24 25 26 Beside other factors, MPD is under investigation as a predictive factor in the development of ARMD.4 15 27 28 29 Growing evidence indicates that oxidative damage contributes to the development of ARM4 30 31 and that MP protects against ARM and ARMD,8 27 32 though the latter remains unproven and is a matter of considerable controversy.33

It is proposed that MP protects the macular region by filtering blue light,34 35 presuming that cumulative ocular exposure to blue light is associated with the prevalence of ARM. Studies with laboratory animals have examined the effect of cumulative photochemical damage, and it has been shown that the threshold for retinal damage induced by different wavelengths of light falls exponentially with decreasing wavelength.36 Moreover, it has been shown that the pattern of light-induced retinal damage is similar to the pattern of degenerative changes observed in human eyes with ARMD. However, measuring lifetime light exposure in humans is difficult; therefore, epidemiologic evidence remains incomplete.37 38 In addition to its blue light-filtering properties, the MP is capable of scavenging free radicals.32 In the photoreceptor outer segments, the antioxidant effect of lutein and zeaxanthin may be an important mechanism.4 39 Antioxidant properties enable the carotenoids to quench singlet oxygen.

We have examined a group of 118 healthy subjects with various ethnic phenotypes to obtain functional maps of MPD based on autofluorescence images.22 We quantified mean macular pigment density (MPDc) in a 1°-diameter circle centered on the fovea.

We found significant differences among MPDc values between the groups of WNH and African subjects. MPDc in WNH subjects (0.36 ± 0.13 DU) was significantly lower than in African subjects (MPDc 0.59 ± 0.14 DU).

What actors could contribute to our observation of significant differences in MPD between the WNH and the African subjects? First, in view of recent observations that genetic variants contribute a highly significant risk for ARMD in white persons, it may be that also in African persons genetic variants will be found that confer protection. Thus, genetics may underlie the observed "ethnicity." Second, exogenous factors, such as diet, smoking, and possibly inflammatory components resulting from systemic or ocular diseases, may influence pigment density. Additionally, illuminance levels may affect pigment density, possibly regulated by iris color.

Those factors could be the reason ARMD, a disease likely to be enhanced by oxidative damage, is more common in white persons than in persons of African phenotype.14 No studies have been published of the differences in MPDc values or MP spatial distribution between ethnic groups. Most studies of MP were conducted primarily in WNH subjects and included only a few Asian subjects.18 19 Yet, ethnicity may play a role in MPDc values. The MPDc value is known to vary with diet and iris color. Given these factors, it is reasonable to speculate that MPDc might vary with ethnicity as far as lifestyle is concerned. However, it is difficult to compare MPDc across studies because of the different methodological set-ups and procedures used. By comparing the foveal luminosity function of Egyptian subjects with those of Western subjects, Isahak speculated that Egyptians might have higher MPDc.40 Hammond et al.41 and Hammond and Caruso-Avery42 report a higher MPDc in subjects with dark irises. Our findings of differences among MPDc values between the studied ethnic groups may be a result of environmental factors, genetic influences, or dietary habits. Hammond42 speculated that a shared tendency might have developed to accumulate melanin of the iris and carotenoids in the retina because of similar environmental factors (e.g., light and oxygen).

Could increased retinal illuminance resulting from light iris color contribute to a depletion of MP? In other words, can light exposure alter the molecular structure so that the antioxidants lutein and zeaxanthin are consumed and metabolized into nonprotective chemical forms? The blue light-filtering effect of lutein and zeaxanthin, found in Henle fibers of the fovea, is a passive function. It is thought to reduce blue light exposure and, with that, the formation of reactive radicals.43 However, lutein and zeaxanthin are present in rod outer segments44 (and potentially cones) and are thought to act directly as antioxidants. Several mechanisms of action are possible, some of which would deplete the original molecules. A detailed discussion of such mechanisms is given in Krinsky.43 Furthermore, the physiological turnover of rod and cone outer segments with shedding of disks from the tips and renewal at the base necessitate the replenishment of outer segment components, including lutein and zeaxanthin. In vitro studies by Kim et al.45 indicate that lutein and zeaxanthin provide good protection against oxidative stress induced by the retinoid derivatives A2PE and A2E. Both molecules act as blue light filters and as antioxidants and are not depleted while exerting their filtering and antioxidant effects. However, chronic exposure to very high oxygen levels, as found in photoreceptors concomitant with presumed increased bright light exposure resulting from light iris color, cannot be compared directly in a short-term in vitro study.

In our opinion the different distribution types of MP with significant ethnic differences could indicate the genetic effect of ARMD prevalence.

The maximum parafoveal ring found was 0.66° ± 0.13° from the fovea. Delori et al.16 found, in more than half their subjects, an annulus of higher density superimposed on a central monotonic-like distribution. This annulus was located 0.7° from the fovea. There were no differences in the localization of the ring maximum between African subjects and WNH subjects. However, we found significant differences of the width at a half maximum between the groups, showing a broader distribution in African subjects. These differences may be caused by the anatomic width of the fovea, which may be associated with race.

We calculated the ratio MPD05–1/MPDc to assess the significance of the parafoveal ring. Theoretically, higher values of MPD05–1/MPDc indicate a more prominent parafoveal ring, whereas lower values show a peak-like distribution. We found significant differences for the ratio MPD05–1/MPDc between the ethnic groups, confirming the presence of race-associated differences in the MP distribution.

Our results were analyzed in light of gender and age dependence and of ethnic distribution. We found no evident gender-related, age-related, or risk factor (e.g., smoking, family history of ARMD)-associated difference in MPDc. This is in agreement with findings of other groups.8 21 46

Mean MPDc measured within a 0.5°-diameter circle centered on the fovea may not represent the protective properties of MP. As in previous studies,21 47 48 49 we observed a large variability of mean MPDc and the distribution of MP around the fovea. We found a high degree of intersubject variability in the lateral extent and shape of distribution of MPDc. Distribution profiles varied from broad distribution with low peaks to sharp, cusped peaks with different widths. Given that the total amount of MP cannot always be predicted from the mean MPDc, as calculated in our study, bias can occur if the lateral extent and shape of distribution are unaccounted for.49


    Acknowledgements
 
The authors thank Henrike Wüstemeier, Cornelia Jahn, Sabine Silva, and Christian Brinkmann for the many ways in which they prepared the project. They also thank Charlotte Remé for her critical discussions and contributions to the manuscript.


    Footnotes
 
Supported by the Swiss National Science Foundation (Grant SNF 3200 Bo-109962/1) and the Velux Foundation Zürich (Grant Velux 303).

Submitted for publication October 10, 2006; revised March 22, 2007; accepted May 30, 2007.

Disclosure: U.E.K. Wolf-Schnurrbusch, None; N. Röösli, None; E. Weyermann, None; M.R. Heldner, None; K. Höhne, None; S. Wolf, None

The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

Corresponding author: Sebastian Wolf, Klinik und Poliklinik für Augenheilkunde, Inselspital, University Bern, CH-3010 Bern, Switzerland; sebastian.wolf{at}insel.ch.


    References
 Top
 Abstract
 Materials and Methods
 Results
 Discussion
 References
 

  1. Pauleikhoff D, Barondes M, Minassian D, Chisholm I, Bird A. Drusen as risk factors in age related macular disease. Am J Ophthalmol. 1990;109:38–43.[Web of Science][Medline][Order article via Infotrieve]
  2. Pauleikhoff D, Chen J, Chisholm I, Bird A. Choroidal perfusion abnormality with age-related Bruch’s membrane change. Am J Ophthalmol. 1990;109:211–217.[Web of Science][Medline][Order article via Infotrieve]
  3. Landrum JT, Bone RA, Joa H, Kilburn MD, Moore LL, Sprague KE. A one year study of the macular pigment: the effect of 140 days of a lutein supplement. Exp Eye Res. 1997;65:57–62.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  4. Beatty S, Boulton M, Henson D, Koh HH, Murray IJ. Macular pigment and age related macular degeneration. Br J Ophthalmol. 1999;83:867–877.[Free Full Text]
  5. Cai J, Nelson DE, Wu M, Sternberg P, Jones DP. Oxidative damage and protection of the RPE. Prog Retinal Eye Res. 2000;19:205–221.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  6. Bird AC, Bressler NM, Bressler SB, et al. An international classification and grading system for age-related maculopathy and age-related macular degeneration. Surv Ophthalmol. 1995;39:367–374.[Web of Science][Medline][Order article via Infotrieve]
  7. van Leeuwen R, Klaver CCW, Vingerling JR, Hofman A, de Jong P. The risk and natural course of age-related maculopathy. Arch Ophthalmol. 2003;121:519–526.[Abstract/Free Full Text]
  8. Beatty S, Murray IJ, Henson DB, Carden D, Koh H-H, Boulton ME. Macular pigment and risk for age-related macular degeneration in subjects from a northern European population. Invest Ophthalmol Vis Sci. 2001;42:439–446.[Abstract/Free Full Text]
  9. Schachat AP, Hyman L, Leske MC, Connell MS, Wu SY, Group BES. Features of age-related macular degeneration in a black population. Arch Ophthalmol. 1995;113:728–735.[Abstract/Free Full Text]
  10. Clemons TE, Milton RC, Klein R, Seddon JM, Ferris FL, 3rd. Risk factors for the incidence of Advanced Age-Related Macular Degeneration in the Age-Related Eye Disease Study (AREDS) AREDS report no. 19. Ophthalmology. 2005;112:533–539.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  11. Congdon N, O’Colmain B, Klaver CC, et al. Causes and prevalence of visual impairment among adults in the United States. Arch Ophthalmol. 2004;122:477–485.[Abstract/Free Full Text]
  12. Despriet DD, Klaver CC, Witteman JC, et al. Complement factor H polymorphism, complement activators, and risk of age-related macular degeneration. JAMA. 2006;296:301–309.[Abstract/Free Full Text]
  13. Kardys I, Klaver CC, Despriet DD, et al. A common polymorphism in the complement factor H gene is associated with increased risk of myocardial infarction: the Rotterdam Study. J Am Coll Cardiol. 2006;47:1568–1575.[Abstract/Free Full Text]
  14. Sommer A, Tielsch JM, Katz J, et al. Racial differences in the cause-specific prevalence of blindness in east Baltimore. N Engl J Med. 1991;325:1412–1417.[Abstract]
  15. Jahn C, Wustemeyer H, Brinkmann C, Trautmann S, Mossner A, Wolf S. Macular pigment density in age-related maculopathy. Graefes Arch Clin Exp Ophthalmol. 2005;243:222–227.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  16. Delori FC, Goger DG, Keilhauer C, Salvetti P, Staurenghi G. Bimodal spatial distribution of macular pigment: evidence of a gender relationship. J Opt Soc Am A Opt Image Sci Vis. 2006;23:521–538.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  17. Berendschot TT, van Norren D. Macular pigment shows ringlike structures. Invest Ophthalmol Vis Sci. 2006;47:709–714.[Abstract/Free Full Text]
  18. Lam RF, Rao SK, Fan DS, Lau FT, Lam DS. Macular pigment optical density in a Chinese sample. Curr Eye Res. 2005;30:799–805.[Web of Science][Medline][Order article via Infotrieve]
  19. Tang CY, Yip HS, Poon MY, Yau WL, Yap MK. Macular pigment optical density in young Chinese adults. Ophthalmic Physiol Opt. 2004;24:586–593.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  20. Wüstemeyer H, Jahn C, Nestler A, Barth T, Wolf S. A new instrument for the quantification of macular pigment density: first results in patients with AMD and healthy subjects. Graefe’s Arch Clin Exp Ophthalmol. 2002;240:666–671.[Web of Science][Medline][Order article via Infotrieve]
  21. Delori FC, Goger DG, Hammond BR, Snodderly DM, Burns SA. Macular pigment density measured by autofluorescence spectrometry: comparison with reflectometry and heterochromatic flicker photometry. J Opt Soc Am. 2001;18:1212–1130.
  22. Wüstemeyer H, Moessner A, Jahn C, Wolf S. Macular pigment density in healthy subjects quantified with a modified confocal scanning laser ophthalmoscope. Graefe’s Arch Clin Exp Ophthalmol. 2003;241:647–651.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  23. Delcourt C, Cristol JP, Tessier F, Leger CL, Descomps B, Papoz L. Age-related macular degeneration and antioxidant status in the POLA study: POLA Study Group. Pathologies Oculaires Liees a l’Age. Arch Ophthalmol. 1999;117:1384–1390.[Abstract/Free Full Text]
  24. Klein R, Klein BEK, Jensen SC. The relation of cardiovascular disease and its risk factors to the 5-year incidence of age-related maculopathy: the Beaver Dam Eye Study. Ophthalmology. 1997;104:1804–1812.[Web of Science][Medline][Order article via Infotrieve]
  25. The Eye Disease Case Control Study G. Risk factors for neovascular age-related macular degeneration. Arch Ophthalmol. 1992;110:1701–1708.[Abstract/Free Full Text]
  26. McCarty CA, Mukesh BN, Fu CL. Risk factors for age-related maculopathy. Arch Ophthalmol. 2001;119:1455–1462.[Abstract/Free Full Text]
  27. Snodderly DM. Evidence for protection against age-related macular degeneration by carotenoids and antioxidant vitamins. Am J Clin Nutr. 1995;62(suppl)1448S–1461S.[Medline][Order article via Infotrieve]
  28. Berendschot TT, Goldbohm RA, Klopping WA, van de Kraats J, van Norel J, van Norren D. Influence of lutein supplementation on macular pigment, assessed with two objective techniques. Invest Ophthalmol Vis Sci. 2000;41:3322–3326.[Abstract/Free Full Text]
  29. Bernstein PS, Yoshida MD, Katz NB, McClane RW, Gellermann W. Raman detection of macular carotenoid pigments in intact human retina. Invest Ophthalmol Vis Sci. 1998;39:2003–2011.[Abstract/Free Full Text]
  30. De La Paz MA, Anderson RE. Lipid peroxidation in rod outer segments: role of hydroxyl and lipid hydroperoxides. Invest Ophthalmol Vis Sci. 1992;33:2091–2096.[Abstract/Free Full Text]
  31. Young RW. Pathophysiology of age-related macular degeneration. Surv Ophthalmol. 1987;31:291–306.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  32. Khachik F, Bernstein PS, Garland DL. Identification of lutein and zeaxanthin oxidation products in and monkey retinas. Invest Ophthalmol Vis Sci. 1997;38:1802–1811.[Abstract/Free Full Text]
  33. Mares-Perlman JA, Brady WE, Klein R, Vanden Langenberg GM, Klein BE, Palta M. Dietary fat and age-related maculopathy. Arch Ophthalmol. 1995;113:743–748.[Abstract/Free Full Text]
  34. Bone RA, Landrum JT, Cains A. Optical density spectra of the macular pigment in vivo and in vitro. Vision Res. 1992;32:105–110.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  35. Sharpe LT, Stockman A, Knau H, Jagle H. Macular pigment densities derived from central and peripheral spectral sensitivity differences. Vision Res. 1998;38:3233–3239.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  36. Ham WTJ, Mueller HA, Sliney DH. Retinal sensitivity to damage from short wavelength light. Nature. 1976;260:153–155.[CrossRef][Medline][Order article via Infotrieve]
  37. Evans JR. Risk factors for age-related macular degeneration. Prog Retinal Eye Res. 2001;20:227–253.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  38. Beatty S, Koh H-H, Henson DB, Boulton ME. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol. 2000;45:115–134.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  39. Rapp LM, Maple SS, Choi JH. Lutein and zeaxanthin concentrations in rod outer segment membranes from perifoveal and peripheral human retina. Invest Ophthalmol Vis Sci. 2000;41:1200–1209.[Abstract/Free Full Text]
  40. Ishak IGH. The photopic luminosity curve for a group of fifteen Egyptian trichomats. J Opt Soc Am. 1952;42:529–534.
  41. Hammond BR, Jr, Wooten BR, Snodderly DM. Cigarette smoking and retinal carotenoids: implications for age-related macular degeneration. Vision Res. 1996;36:3003–3009.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  42. Hammond BR, Jr, Wooten BR, Curran-Celentano J. Carotenoids in the retina and lens: possible acute and chronic effects on human visual performance. Arch Biochem Biophys. 2001;385:41–46.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  43. Krinsky NI, Landrum JT, Bone RA. Biologic mechanisms of the protective role of lutein and zeaxanthin in the eye. Annu Rev Nutr. 2003;23:171–201.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  44. Rapp LM, Maple SS, Choi JH. Lutein and zeaxanthin concentrations in rod outer segment membranes from perifoveal and peripheral human retina. Invest Ophthalmol Vis Sci. 2000;41:1200–1209.[Abstract/Free Full Text]
  45. Kim SR, Nakanishi K, Itagaki Y, Sparrow JR. Photooxidation of A2-PE, a photoreceptor outer segment fluorophore, and protection by lutein and zeaxanthin. Exp Eye Res. 2006;82:828–839.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  46. Berendschot TT, Willemse-Assink JJ, Bastiaanse M, de Jong PT, van Norren D. Macular pigment and melanin in age-related maculopathy in a general population. Invest Ophthalmol Vis Sci. 2002;43:1928–1932.[Abstract/Free Full Text]
  47. Hammond C, Webster A, Snieder H, Bird AC, Gilbert C, Spector T. Genetic influence on early age-related maculopathy: a twin study. Ophthalmology. 2002;109:730–736.[CrossRef][Web of Science][Medline][Order article via Infotrieve]
  48. Berendschot TT, Broekmans WM, Klopping-Ketelaars IA, Kardinaal AF, Van Poppel G, Van Norren D. Lens aging in relation to nutritional determinants and possible risk factors for age-related cataract. Arch Ophthalmol. 2002;120:1732–1737.[Abstract/Free Full Text]
  49. Robson AG, Moreland JD, Pauleikhoff D, et al. Macular pigment density and distribution: comparison of fundus autofluorescence with minimum motion photometry. Vision Res. 2003;43:1765–1775.[CrossRef][Web of Science][Medline][Order article via Infotrieve]



This article has been cited by other articles:


Home page
Br. J. Ophthalmol.Home page
A Ayata, S Tatlipinar, M Unal, D Ersanli, and A H Bilge
Excitation-time-dependent increment in the luminescence of fundus autofluorescence
Br. J. Ophthalmol., September 1, 2008; 92(9): 1241 - 1243.
[Abstract] [Full Text] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (3)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Wolf-Schnurrbusch, U. E. K.
Right arrow Articles by Wolf, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Wolf-Schnurrbusch, U. E. K.
Right arrow Articles by Wolf, S.


HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS