The rationale and evidence base for a protective role of macular pigment in age-related maculopathy

British Journal of Ophthalmology

Volumn 92, Issue 9, 2008, Pages 1163-1168

  Loane, E ^a   Kelliher, C ^b   Beatty, S ^a,b   Nolan, J M ^a  

^a Ireland   (Ireland)

^b WATERFORD REGIONAL HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; MACULAR PIGMENT LUTEIN; MACULAR PIGMENT ZEAXANTHIN; UNCLASSIFIED DRUG;

CLINICAL FEATURE; DIET SUPPLEMENTATION; DISEASE COURSE; HUMAN; OBSERVATIONAL STUDY; OXIDATIVE STRESS; PREVENTION AND CONTROL; PRIORITY JOURNAL; RETINA MACULA AGE RELATED DEGENERATION; REVIEW; VITAMIN SUPPLEMENTATION;

AGED; ANTIOXIDANTS; CAROTENOIDS; DIETARY SUPPLEMENTS; EVIDENCE-BASED MEDICINE; FEMALE; HUMANS; MACULA LUTEA; MACULAR DEGENERATION; MALE; MIDDLE AGED; OXIDATIVE STRESS; RETINAL PIGMENTS;

EID: 51149118038     PISSN: 00071161     EISSN: None     Source Type: Journal    
DOI: 10.1136/bjo.2007.135566     Document Type: Review

References (95)

1. Bressler NM. Age-related macular degeneration is the leading cause of blindness. JAMA 2004;291:1900-1.
2. Congdon NG, Friedman DS, Lietman T. Important causes of visual impairment in the world today. JAMA 2003;290:2057-60.
3. Bunce C, Wormald R. Causes of blind certifications in England and Wales: April 1999-March 2000. Eye. In press.
4. Kelliher C, Kenny D, O'Brien C. Trends in blind registration in the adult population of the Republic of Ireland 1996-2003. Br J Ophthalmol 2006;90:367-71.
5. van LR, Klaver CC, Vingerling JR, et al. Epidemiology of age-related maculopathy: a review. Eur J Epidemiol 2003;18:845-54.
6. Augustin A, Sahel JA, Bandello F, et al. Anxiety and depression prevalence rates in age-related macular degeneration. Invest Ophthalmol Vis Sci 2007;48:1498-503.
7. Bandello F, Lafuma A, Berdeaux G. Public health impact of neovascular age-related macular degeneration treatments extrapolated from visual acuity. Invest Ophthalmol Vis Sci 2007;48:96-103.
8. Sommerburg O, Keunen JEE, Bird AC, et al. Fruits and vegetables that are sources for lutein and zeaxanthin: the macular pigment in human eyes. Br J Ophthalmol 1998;82:907-10.
9. Maoka T, Arai A, Shimizu M, et al. The first isolation of enantiomeric and mesozeaxanthin in nature. Comp Biochem Physiol B 1986;83:121-4.
10. Beatty S, Koh HH, Henson D, et al. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 2000;45:115-34.
11. Schork NJ. Genetics of complex disease: approaches, problems, and solutions. Am J Respir Crit Care Med 1997;156:103-9S.
12. Klein R, Klein BEK, Moss SE. Relation of smoking to the incidence of age-related maculopathy-The Beaver Dam Eye Study. Am J Epidemiol 1998;147:103-10.
13. Tan JS, Mitchell P, Kifley A, et al. Smoking and the long-term incidence of age-related macular degeneration: the Blue Mountains Eye Study. Arch Ophthalmol 2007;125:1089-95.
14. Chakravarthy U, Augood C, Bentham GC, et al. Cigarette smoking and age-related macular degeneration in the EUREYE Study. Ophthalmology 2007;114:1157-63.
15. Tomany SC, Cruickshanks KJ, Klein R, et al. Sunlight and the 10-year incidence of age-related maculopathy-The Beaver Dam eye study. Arch Ophthalmol 2004;122:750-7.
16. SanGiovanni JP, Chew EY, Clemons TE, et al. The relationship of dietary carotenoId and vitamin A, E, and C intake with age-related macular degeneration in a case-control study: AREDS Report No. 22. Arch Ophthalmol 2007;125:1225-32.
17. McCord JM. The evolution of free radicals and oxidative stress. Am J Med 2000;108:652-9.
18. Suzuki M, Kamei M, Itabe H, et al. Oxidized phospholipids in the macula increase with age and in eyes with age-related macular degeneration. Mol Vis 2007;13:772-8.
19. Lu L, Hackett SF, Mincey A, et al. Effects of different types of oxidative stress in RPE cells. J Cell Physiol 2006;206:119-25.
20. Sundelin S, Wihlmark U, Nilsson SE, et al. Lipofuscin accumulation in cultured retinal pigment epithelial cells reduces their phagocytic capacity. Curr Eye Res 1998;17:851-7.
21. Kennedy CJ, Rakoczy PE, Constable IJ. Lipofuscin of the retinal pigment epithelium: a review. Eye 1995;9:763-71.
22. Algvere PV, Marshall J, Seregard S. Age-related maculopathy and the impact of blue light hazard. Acta Ophthalmol Scand 2006;84:4-15.
23. Wu J, Seregard S, Algvere PV. Photochemical damage of the retina. Surv Ophthalmol 2006;51:461-81.
24. Noell WK, Walker VS, Kang BS, et al. Retinal damage by light in rats. Invest Ophthalmol 1966;5:450-73.
25. Imamura Y, Noda S, Hashizume K, et al. Drusen, choroidal neovascularization, and retinal pigment epithelium dysfunction in S0D1-deficient mice: a model of age-related macular degeneration. Proc Natl Acad Sci U S A 2006;103:11282-7.
26. Boulton M, Dontsov A, Jarvisevans J, et al. Lipofuscin is a photoinducible free-radical generator. J Photochem Photobiol B-Biol 1993;19:201-4.
27. Rozanowska M, Wessels J, Boulton M, et al. Blue light-induced singlet oxygen generation by retinal lipofuscin in non-polar media. Free Bad Biol Med 1998; 24:1107-12.
28. Shaban H, Borras C, Vina J, et al. Phosphatidylglycerol potently protects human retinal pigment epithelial cells against apoptosis induced by A2E, a compound suspected to cause age-related macula degeneration. Exp Eye Res 2002;75:99-108.
29. Sparrow JR, Vollmer-Snarr HR, Zhou J, et al. A2E-epoxides damage DNA in retinal pigment epithelial cells. Vitamin E and other antioxidants inhibit A2E-epoxide formation. J Biol Chem 2003;278:18207-13.
30. Bone RA, Landrum JT, Hime GW, et al. Stereochemistry of the human macular carotenoids. Invest Ophthalmol Vis Sci 1993;34:2033-40.
31. Bone RA, Landrum JT, Tarsis SL. Preliminary identification of the human macular pigment. Vision Res 1985;25:1531-5.
32. Neuringer M, Sandstrom MM, Johnson EJ, et al. Nutritional manipulation of primate retinas, I: effects of lutein or zeaxanthin supplements on serum and macular pigment in xanthophyll-free rhesus monkeys. Invest Ophthalmol Vis Sci 2004;45:3234-43.
33. Nebeling LC, Forman MR, Graubard Bl, et al. Changes in carotenoid intake in the United States: The 1987 and 1992 National Health Interview Surveys. J Am Diet Assoc 1997;97:991-6.
34. Nebeling LC, Forman MR, Graubard Bl, et al. The impact of lifestyle characteristics on carotenoid intake in the United States: The 1987 National Health Interview Survey. Am J Publ Health 1997;87:268-71.
35. Snodderly DM, Auran JD, Delori FC. The macular pigment. II. Spatial distribution in primate retinas. Invest Ophthalmol Vis Sci 1984;25:674-85.
36. Bone RA, Landrum JT, Fernandez L, et al. Analysis of the macular pigment by HPLC-Retinal distribution and age study. Invest Ophthalmol Vis Sci 1988;29:843-9.
37. Snodderly DM, Handelman GJ, Adler AJ. Distribution of individual macular pigment carotenoids in central retina of macaque and squirrel monkeys. Invest Ophthalmol Vis Sci 1991;32:268-79.
38. Bone RA, Landrum JT, Friedes LM, et al. Distribution of lutein and zeaxanthin stereoisomers in the human retina. Exp Eye Res 1997;64:211-18.
39. Hammond BR, Wooten BR, Snodderly DM. Individual variations in the spatial profile of human macular pigment. J Opt Soc Am A Optics Image Sci Vis 1997;14:1187-96.
40. Sommerburg O, Siems WG, van Kuijk FJ. Localization of carotenoids in different eye tissues. Biofactors 2000;11:3-6.
41. Bernstein PS, Balashov NA, Tsong ED, et al. Retinal tubulin binds macular carotenoids. Invest Ophthalmol Vis Sci 1997;38:167-75.
42. 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;41:1200-9.
43. Bhosale P, Larson AJ, Frederick JM, et al. Identification and characterization of a Pi isoform of glutathione S-transferase (GSTP1) as a zeaxanthin-binding protein in the macula of the human eye. J Biol Chem 2004;279:49447-54.
44. Trieschmann M, van Kuijk FJ, Alexander R, et al. Macular pigment in the human retina: histological evaluation of localization and distribution. Eye. In press.
45. Sujak A, Gabrielska J, Grudzinski W, et al. Lutein and zeaxanthin as protectors of lipid membranes against oxidative damage: The structural aspects. Arch Biochem Biophys 1999;371:301-7.
46. Bhosale P, Bernstein PS. Synergistic effects of zeaxanthin and its binding protein in the prevention of lipid membrane oxidation. Biochim Biophys Acta 2005; 1740:116-21.
47. Trevithick-Sutton CC, Foote CS, Collins M, et al. The retinal carotenoids zeaxanthin and lutein scavenge superoxide and hydroxyl radicals: a chemiluminescence and ESR study. Mol Vis 2006;12:1127- 35.
48. Kim SR, Nakanishi K, Itagaki Y, et al. Photooxidation of A2-PE, a photoreceptor outer segment fluorophore, and protection by lutein and zeaxanthin. Exp Eye Res 2006;82:828-39.
49. Wrona M, Rozanowska M, Sarna T. Zeaxanthin in combination with ascorbic acid or alpha-tocopherol protects ARPE-19 cells against photosensitized peroxidation of lipids. Free Rad Biol Med 2004;36:1094-101.
50. Kirschfeld K. Carotenoid pigments: their possible role in protecting against photooxidation in eyes and photoreceptor cells. Proc R Soc Lend B Biol Sci 1982;216:71-85.
51. Khachik F, Bernstein PS, Garland DL. Identification of lutein and zeaxanthin oxidation products in human and monkey retinas. Invest Ophthalmol Vis Sci 1997;38:1802-11.
52. Siems WG, Sommerburg O, van Kuijk FJ. Lycopene and beta-carotene decompose more rapidly than lutein and zeaxanthin upon exposure to various pro-oxidants in vitro Biofactors 1999;10:105-13.
53. Cantrell A, McGarvey DJ, Truscott TG, et al. Singlet oxygen quenching by dietary carotenoids in a model membrane environment. Arch Biochem Biophys 2003;412:47-54.
54. Thomson LR, Toyoda Y, Langner A, et al. Elevated retinal zeaxanthin and prevention of light-induced photoreceptor cell death in quail. Invest Ophthalmol Vis Sci 2002;43:3538 49.
55. Chucair AJ, Rotstein NP, SanGiovanni JP, et al. Lutein and zeaxanthin protect photoreceptors from apoptosis induced by oxidative stress: relation with docosahexaenoic acid. Invest Ophthalmol Vis Sci 2007;48:5168-77.
56. Kalariya NM, Ramana KV, Srivastava SK, et al. Carotenoid derived aldehydes-induced oxidative stress causes apoptotic cell death In human retinal pigment epithelial cells. Exp Eye Res 2008;86:70-80.
57. Junghans A, Sies H, Stahl W. Macular pigments lutein and zeaxanthin as blue light filters studied in liposomes. Arch Biochem Biophys 2001;391:160-4.
58. Stringham JM, Hammond BR, Wooten BR, et al. Compensation for light loss resulting from filtering by macular pigment: relation to the S-cone pathway. Optom Vis Sci 2006;83:887-94.
59. Mares-Perlman JA, Fisher Al, Klein R, et al. Lutein and zeaxanthin in the diet and serum and their relation to age-related maculopathy in the Third National Health and Nutrition Examination Survey. Am J Epidemiol 2001;153:424-32.
60. Mares-Perlman JA, Klein R, Klein BEK, et al. Association of zinc and antioxidant nutrients with age-related maculopathy. Arch Ophthalmol 1996;114:991-7.
61. Seddon JM, Ajani UA, Sperduto RD. Dietary carotenoids, vitamins A, C, and E, and advanced age-related macular degeneration. JAMA 1994;272:1413-20.
62. VandenLangenberg GM, Mares-Perlman JA, Klein R, et al. Associations between antioxidant and zinc intake and the 5-year incidence of early age-related maculopathy in the Beaver Dam Eye Study. Am J Epidemiol 1998;148:204-14.
63. Smith W, Mitchell P, Webb K, et al. Dietary antioxidants and age-related maculopathy-The Blue Mountains Eye Study. Ophthalmology 1999;106:761-7.
64. Flood V, Wang JJ, Manzi F, et al. Dietaty antioxidant intake and incidence of early age-related maculopathy: the Blue Mountains Eye Study. Ophthalmology 2002;109:2272-8.
65. Cho EY, Seddon JM, Rosner B, et al. Prospective study of intake of fruits, vegetables, vitamins, and carotenoids and risk of age-related maculopathy. Arch Ophthalmol 2004;122:883-92.
66. Goldberg J, Flowerdrew G, Smith E. Factors associated with age-related macular degeneration-analysis of data from NHANES I. Am J Epidemiol 1998;128:700-11.
67. Snellen ELM, Verbeek ALM, van den Hoogen GWP, et al. Neovascular age-related macular degeneration and Its relationship to antioxidant intake, Acta Ophthalmol Scand 2002;80:368-71.
68. Tan JS, Wang JJ, Flood V, et al. Dietary antioxidants and the long-term incidence of age-related macular degeneration. The Blue Mountains Eye Study, Ophthalmology 2008;115:334-41.
69. Chong EW, Wong TY, Kreis AJ, et al. Dietary antioxidants and primary prevention of age related macular degeneration: systematic review and meta-analysis. BMJ 2007;335:755.
70. van LR, Boekhoorn S, Vingerling JR, et al. Dietary intake of antioxidants and risk of age-related macular degeneration. JAMA 2005;294:3101-7.
71. Moeller SM, Parekh N, Tinker L, et al. Associations between intermediate age-related macular degeneration and lutein and zeaxanthin in the Carotenoids in Age-related Eye Disease Study (CAREDS); ancillary study of the Women's Health Initiative. Arch Ophthalmol 2006;124:1151-62.
72. Cho E, Seddon JM, Rosner B, et al. Prospective study of Intake of fruits, vegetables, vitamins, and carotenoids and risk of age-related maculopathy. Arch Ophthalmol 2004;122:883-92.
73. Blumenkranz MS, Russell SR, Robey MG, et al. Risk-factors in age-related maculopathy complicated by choroidal neovascularization. Ophthalmology 1986;93:552-8.
74. Yannuzzi LA, Sorenson JA, Sobel RS, et al. Risk-factors for neovascular age-related macular degeneration. Arch Ophthalmol 1992;110:1701-8.
75. Gale CR, Hall NF, Phillips DIW, et al. Lutein and zeaxanthin status and risk of age-related macular degeneration. Invest Ophthalmol Vis Sci 2003;44:2461-5.
76. Sperduto RD. Antioxidant status and neovascular age-related macular degeneration. Arch Ophthalmol 1993;111:104-9.
77. Mares-Perlman JA, Brady WE, Klein R, et al. Serum antioxidants and age-related macular degeneration in a population based case control study. Arch Ophthalmol 1995;113:1518 23.
78. Delcourt C, Cristol JP, Tessier F, et al. Age-related macular degeneration and antioxidant status in the POLA study. Arch Ophthalmol 1999;117:1384-90.
79. Smith W, Mitchell P, Rochester C. Serum beta carotene, alpha tocopherol, and age-related maculopathy: the Blue Mountains Eye Study. Am J Ophthalmol 1997;124:838-40.
80. Aoki K, Ito Y, Sasaki R, et al. Smoking, alcohol drinking and serum carotenoids levels. Japan J Cancer Res 1987;78:1049-56.
81. West S, Vitale S, Hallfrisch J, et al. Are antioxidants or supplements protective for age-related macular degeneration? Arch Ophthalmol 1994;112:222-7.
82. Belda Jl, Roma J, Vilela C, et al. Serum vitamin E levels negatively correlate with severity of age-related macular degeneration. Mech Ageing Dev 1999;107:159-64.
83. Tsang NC, Penfold PL, Snitch PJ, et al. Serum levels of antioxidants and age-related macular degeneration. Doc Ophthalmol 1992;81:387-400.
84. Nolan JM, Stack J, O' Donovan O, et al. Risk factors for age-related maculopathy are associated with a relative lack of macular pigment. Exp Eye Res 2007;84:61-74.
85. Koh HH, Murray IJ, Nolan D, et al. Serum and macular responses to lutein supplement in subjects with and without age-related maculopathy: a pilot study. Exp Eye Research 2004;79:21-7.
86. Richer S, Devenport J, Lang JC. LAST II: Differential temporal responses of macular pigment optical density in patients with atrophic age-related macular degeneration to dietary supplementation with xanthophylls. Optometry 2007;78:213-19.
87. Trieschmann M, Beatty S, Nolan JM, et al. Changes in macular pigment optical density and serum concentrations of Its constituent carotenoids following supplemental lutein and zeaxanthin: the LUNA study. Exp Eye Res 2007;84:718-28
88. Taylor HR, Tikellis G, Robman LD, et al. Vitamin E supplementation and macular degeneration: randomised controlled trial. Br Med J 2002;325:11-14.
89. Teikari JM, Laatikainen L, Virtamo J, et al. Six-year supplementation with alpha-tocopherol and beta-carotene and age-related maculopathy. Acta Ophthalmol Scand 1998;76:224-9.
90. Kassoff A, Kassoff J, Buehler J, et al. A randomized, placebo-controlled, clinical trial of high-dose supplementation with vitamins C and E, beta carotene, and zinc for age-related macular degeneration and vision loss-AREDS Report No, 8. Arch Ophthalmol 2001;119:1417-36.
91. Richer S. ARMD-pilot (Case series) environmental intervention data. J Am Optom Assoc 1999;70:24-36.
92. Richer S, Stiles W, Statkute L, et al. Double-masked, placebo-controlled, randomized trial of lutein and antioxidant supplementation in the intervention of atrophic age-related macular degeneration: the Veterans LAST study (Lutein Antioxidant Supplementation Trial). Optometry 2004;75:216-30.
93. Neelam K, Hogg RE, Stevenson M, et al. Carotenoids in age-related maculopathy: Design and methods. Ophthalmic Epidemiol. In press.
94. Albanes D, Heinonen OP, Taylor PR, et al. Alpha-Tocopherol and beta-carotene supplements and lung cancer incidence in the alpha-tocopherol, beta-carotene cancer prevention study: effects of base-line characteristics and study compliance. J Natl Cancer Inst 1996;88:1560-70.
95. Anon. Vitamins: what they do and where to find them (EU Food Information Council). http://www.eufic.org/article/en/page/MARCHIVE/ecpid/ miniguide-vitamins/ (accessed 18 Jul 2008).