Markers of inflammation, oxidative stress, and endothelial dysfunction and the 20-year cumulative incidence of early age-related macular degeneration the beaver dam eye study

JAMA Ophthalmology

Volumn 132, Issue 4, 2014, Pages 446-455

  Klein, Ronald ^a   Myers, Chelsea E ^a   Cruickshanks, Karen J ^a   Gangnon, Ronald E ^a   Danforth, Lorraine G ^a   Sivakumaran, Theru A ^b,c   Iyengar, Sudha K ^b   Tsai, Michael Y ^d   Klein, Barbara E K ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 ISOPROSTANE; ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; C REACTIVE PROTEIN; CARBONYL DERIVATIVE; COMPLEMENT COMPONENT C2; COMPLEMENT COMPONENT C3; COMPLEMENT FACTOR H; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; TUMOR NECROSIS FACTOR RECEPTOR 2; VASCULAR CELL ADHESION MOLECULE 1;

ADULT; AGE DISTRIBUTION; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUSEN; ENDOTHELIAL DYSFUNCTION; EYE PHOTOGRAPHY; FEMALE; FOLLOW UP; GENETIC RISK; HIGH RISK POPULATION; HUMAN; INCIDENCE; INFLAMMATION; LEUKOCYTE COUNT; MAJOR CLINICAL STUDY; MALE; OXIDATIVE STRESS; PIGMENT DISORDER; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RETINA MACULA AGE RELATED DEGENERATION; RISK ASSESSMENT; RISK FACTOR; SMOKING; VISUAL SYSTEM EXAMINATION;

ADULT; AGED; AGED, 80 AND OVER; BIOLOGICAL MARKERS; C-REACTIVE PROTEIN; CORNEAL ENDOTHELIAL CELL LOSS; FEMALE; HUMANS; INCIDENCE; INFLAMMATION; INTERLEUKIN-6; LONGITUDINAL STUDIES; MACULAR DEGENERATION; MALE; MIDDLE AGED; OXIDATIVE STRESS; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; RETINAL DRUSEN; RISK ASSESSMENT; VASCULAR CELL ADHESION MOLECULE-1; WISCONSIN;

EID: 84898639156     PISSN: 21686165     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamaophthalmol.2013.7671     Document Type: Article

References (78)

1. Ferris FL III, Tielsch JM. Blindness and visual impairment: a public health issue for the future as well as today. Arch Ophthalmol. 2004; 122 (4): 451-452.
2. Friedman DS, O'Colmain BJ, Munoz B, et al; Eye Diseases Prevalence Research Group. Prevalence of age-related macular degeneration in the United States. Arch Ophthalmol. 2004; 122 (4): 564-572.
3. Congdon N, O'Colmain B, Klaver CC, et al; Eye Diseases Prevalence Research Group. Causes and prevalence of visual impairment among adults in the United States. Arch Ophthalmol. 2004; 122 (4): 477-485.
4. Haddad S, Chen CA, Santangelo SL, Seddon JM. The genetics of age-related macular degeneration: a reviewof progress to date. Surv Ophthalmol. 2006; 51 (4): 316-363.
5. Scholl HP, Fleckenstein M, Charbel Issa P, Keilhauer C, Holz FG, Weber BH. An update on the genetics of age-related macular degeneration. Mol Vis. 2007; 13: 196-205.
6. Klein R. Epidemiology of age-related macular degeneration. In: Penfold PL, Provis JM, eds. Macular Degeneration: Science and Medicine in Practice. Berlin, Germany: Springer-Verlag; 2005: 79-101.
7. Sarks SH. Ageing and degeneration in the macular region: a clinico-pathological study. Br J Ophthalmol. 1976; 60 (5): 324-341.
8. Penfold PL, Killingsworth MC, Sarks SH. Senile macular degeneration: the involvement of giant cells in atrophy of the retinal pigment epithelium. Invest Ophthalmol Vis Sci. 1986; 27 (3): 364-371.
9. Hageman GS, Luthert PJ, Victor Chong NH, Johnson LV, Anderson DH, Mullins RF. An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch's membrane interface in aging and age-related macular degeneration. Prog Retin Eye Res. 2001; 20 (6): 705-732.
10. Ernst E, Hammerschmidt DE, Bagge U, Matrai A, Dormandy JA. Leukocytes and the risk of ischemic diseases. JAMA. 1987; 257 (17): 2318-2324.
11. Klein RJ, Zeiss C, Chew EY, et al. Complement factor H polymorphism in age-related macular degeneration. Science. 2005; 308 (5720): 385-389.
12. Haines JL, Hauser MA, Schmidt S, et al. Complement factor H variant increases the risk of age-related macular degeneration. Science. 2005; 308 (5720): 419-421.
13. Edwards AO, Ritter R III, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science. 2005; 308 (5720): 421-424.
14. Jarrett SG, BoultonME. Consequences of oxidative stress in age-related macular degeneration. Mol Aspects Med. 2012; 33 (4): 399-417.
15. Cai X, McGinnis JF. Oxidative stress: the Achilles' heel of neurodegenerative diseases of the retina. Front Biosci (Landmark Ed). 2012; 17: 1976-1995.
16. Hollyfield JG. Age-related macular degeneration: the molecular link between oxidative damage, tissue-specific inflammation and outer retinal disease: the Proctor lecture. Invest Ophthalmol Vis Sci. 2010; 51 (3): 1275-1281.
17. Decanini A, Nordgaard CL, Feng X, Ferrington DA, Olsen TW. Changes in select redox proteins of the retinal pigment epithelium in age-related macular degeneration. Am J Ophthalmol. 2007; 143 (4): 607-615.
18. Tsao YP, Ho TC, Chen SL, Cheng HC. Pigment epithelium-derived factor inhibits oxidative stress-induced cell death by activation of extracellular signal-regulated kinases in cultured retinal pigment epithelial cells. Life Sci. 2006; 79 (6): 545-550.
19. Handelman GJ. Evaluation of oxidant stress in dialysis patients. Blood Purif. 2000; 18 (4): 343-349.
20. DaviesMJ, Fu S, Wang H, Dean RT. Stable markers of oxidant damage to proteins and their application in the study of human disease. Free Radic Biol Med. 1999; 27 (11-12): 1151-1163.
21. Sies H. Oxidative stress: oxidants and antioxidants. Exp Physiol. 1997; 82 (2): 291-295.
22. Morrow JD, Frei B, Longmire AW, et al. Increase in circulating products of lipid peroxidation (F2-isoprostanes) in smokers: smoking as a cause of oxidative damage. N Engl J Med. 1995; 332 (18): 1198-1203.
23. Pow DV, Sullivan RK, Williams SM, Wolde Mussie E. Transporters and oxidative stress in AMD. In: Penfold PL, Provis JM, eds. Macular Degeneration: Science and Medicine in Practice. Berlin, Germany: Springer-Verlag; 2005: 123-148.
24. Shaw PX, Zhang L, Zhang M, et al. Complement factor H genotypes impact risk of age-related macular degeneration by interaction with oxidized phospholipids. Proc Natl Acad Sci U S A. 2012; 109 (34): 13757-13762.
25. Lip PL, Blann AD, Hope-Ross M, Gibson JM, Lip GY. Age-related macular degeneration is associated with increased vascular endothelial growth factor, hemorheology and endothelial dysfunction. Ophthalmology. 2001; 108 (4): 705-710.
26. Anderson DH, Mullins RF, Hageman GS, Johnson LV. A role for local inflammation in the formation of drusen in the aging eye. Am J Ophthalmol. 2002; 134 (3): 411-431.
27. Boekhoorn SS, Vingerling JR, Witteman JC, Hofman A, de Jong PT. C-reactive protein level and risk of aging macula disorder: The Rotterdam Study. Arch Ophthalmol. 2007; 125 (10): 1396-1401.
28. Boey PY, Tay WT, Lamoureux E, et al. C-reactive protein and age-related macular degeneration and cataract: the Singapore Malay Eye Study. Invest Ophthalmol Vis Sci. 2010; 51 (4): 1880-1885.
29. Schaumberg DA, ChristenWG, Buring JE, Glynn RJ, Rifai N, Ridker PM. High-sensitivity C-reactive protein, other markers of inflammation, and the incidence of macular degeneration in women. Arch Ophthalmol. 2007; 125 (3): 300-305.
30. Dasch B, Fuhs A, Behrens T, et al. Inflammatory markers in age-related maculopathy: cross-sectional analysis from the Muenster Aging and Retina Study. Arch Ophthalmol. 2005; 123 (11): 1501-1506.
31. Hogg RE, Woodside JV, Gilchrist SE, et al. Cardiovascular disease and hypertension are strong risk factors for choroidal neovascularization. Ophthalmology. 2008; 115 (6): 1046-1052, e2.
32. Seddon JM, George S, Rosner B, Rifai N. Progression of age-related macular degeneration: prospective assessment of C-reactive protein, interleukin 6, and other cardiovascular biomarkers. Arch Ophthalmol. 2005; 123 (6): 774-782.
33. Klein R, Klein BE, Knudtson MD, Wong TY, Shankar A, Tsai MY. Systemic markers of inflammation, endothelial dysfunction, and age-related maculopathy. Am J Ophthalmol. 2005; 140 (1): 35-44.
34. Klein R, Knudtson MD, Klein BE, et al. Inflammation, complement factor h, and age-related macular degeneration: the Multi-ethnic Study of Atherosclerosis. Ophthalmology. 2008; 115 (10): 1742-1749.
35. McGwin G, Hall TA, Xie A, Owsley C. The relation between C reactive protein and age related macular degeneration in the Cardiovascular Health Study. Br J Ophthalmol. 2005; 89 (9): 1166-1170.
36. Mitta VP, ChristenWG, Glynn RJ, et al. C-reactive protein and the incidence of macular degeneration: pooled analysis of 5 cohorts. JAMA Ophthalmol. 2013; 131 (4): 507-513.
37. BrantleyMA Jr, OsbornMP, Sanders BJ, et al. Plasma biomarkers of oxidative stress and genetic variants in age-related macular degeneration. Am J Ophthalmol. 2012; 153 (3): 460-467, e1.
38. Machali?ska A, KawaMP, MarliczW, Machali?ski B. Complement system activation and endothelial dysfunction in patients with age-related macular degeneration (AMD): possible relationship between AMD and atherosclerosis. Acta Ophthalmol. 2012; 90 (8): 695-703.
39. Klein R, Klein BE, Linton KL, DeMets DL. The Beaver Dam Eye Study: visual acuity. Ophthalmology. 1991; 98 (8): 1310-1315.
40. Klein R, Klein BE, Lee KE. Changes in visual acuity in a population: the Beaver Dam Eye Study. Ophthalmology. 1996; 103 (8): 1169-1178.
41. Klein R, Klein BE, Lee KE, Cruickshanks KJ, Chappell RJ. Changes in visual acuity in a population over a 10-year period: the Beaver Dam Eye Study. Ophthalmology. 2001; 108 (10): 1757-1766.
42. Klein R, Klein BE, Lee KE, Cruickshanks KJ, Gangnon RE. Changes in visual acuity in a population over a 15-year period: the Beaver Dam Eye Study. Am J Ophthalmol. 2006; 142 (4): 539-549.
43. Klein R, Lee KE, Gangnon RE, Klein BE. Incidence of visual impairment over a 20-year period: the Beaver Dam Eye Study. Ophthalmology. 2013; 120 (6): 1210-1219.
44. Klein BE, Klein R. The Beaver Dam Eye Study V: Manual of Operations. Springfield, VA: National Technical Information Service; 2010. PB2010-114194.
45. Klein R, Myers CE, Meuer SM, et al. Risk alleles in CFH and ARMS2 and the long-term natural history of age-related macular degeneration: the Beaver Dam Eye Study. JAMA Ophthalmol. 2013; 131 (3): 383-392.
46. Klein R, Davis MD, Magli YL, Segal P, Klein BE, Hubbard L. The Wisconsin Age-Related Maculopathy Grading System. Springfield, VA: National Technical Information Service; 1991. Accession No. PB91-184267.
47. Klein R, Davis MD, Magli YL, Segal P, Klein BE, Hubbard L. The Wisconsin Age-Related Maculopathy Grading System. Ophthalmology. 1991; 98 (7): 1128-1134.
48. Klein R, Klein BE, Linton KL. Prevalence of age-related maculopathy: the Beaver Dam Eye Study. Ophthalmology. 1992; 99 (6): 933-943.
49. Klein R, Klein BE, Jensen SC, Meuer SM. The five-year incidence and progression of age-related maculopathy: the Beaver Dam Eye Study. Ophthalmology. 1997; 104 (1): 7-21.
50. Klein R, Klein BE, Tomany SC, Meuer SM, Huang GH. Ten-year incidence and progression of age-related maculopathy: the Beaver Dam Eye Study. Ophthalmology. 2002; 109 (10): 1767-1779.
51. Klein R, Klein BE, Knudtson MD, Meuer SM, SwiftM, Gangnon RE. Fifteen-year cumulative incidence of age-related macular degeneration: the Beaver Dam Eye Study. Ophthalmology. 2007; 114 (2): 253-262.
52. Klein R, Meuer SM, Myers CE, et al. Harmonizing the classification of age-related macular degeneration in the Three Continent AMD Consortium. Ophthalmic Epidemiol. In press.
53. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J AmStat Assoc. 1958; 53: 457-481.
54. Gooley TA, LeisenringW, Crowley J, Storer BE. Estimation of failure probabilities in the presence of competing risks: new representations of old estimators. Stat Med. 1999; 18 (6): 695-706.
55. Hosmer DWJr, Lemeshow S. Special topics. In: Applied Logistic Regression. New York, NY: John Wiley and Sons; 1989: 238-245.
56. DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988; 44 (3): 837-845.
57. Johnson PT, Betts KE, RadekeMJ, Hageman GS, Anderson DH, Johnson LV. Individuals homozygous for the age-related macular degeneration risk-conferring variant of complement factor H have elevated levels of CRP in the choroid. ProcNatl Acad Sci U S A. 2006; 103 (46): 17456-17461.
58. DeWan A, Bracken MB, Hoh J. Two genetic pathways for age-related macular degeneration. Curr Opin Genet Dev. 2007; 17 (3): 228-233.
59. Perkins SJ, Nan R, Li K, Khan S, Miller A. Complement factor H-ligand interactions: self-association, multivalency and dissociation constants. Immunobiology. 2012; 217 (2): 281-297.
60. Black RA, Doedens JR, Mahimkar R, et al. Substrate specificity and inducibility of TACE (tumour necrosis factor alpha-converting enzyme) revisited: the Ala-Val preference, and induced intrinsic activity. Biochem Soc Symp. 2003; (70): 39-52.
61. de Oliveira Dias JR, Rodrigues EB, Maia M, Magalhaes O Jr, Penha FM, Farah ME. Cytokines in neovascular age-related macular degeneration: fundamentals of targeted combination therapy. Br J Ophthalmol. 2011; 95 (12): 1631-1637.
62. Age-Related Eye Disease Study Research Group. 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 (10): 1417-1436.
63. Beatty S, Koh H, Phil M, Henson D, BoultonM. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol. 2000; 45 (2): 115-134.
64. Cai J, Nelson KC, Wu M, Sternberg P Jr, Jones DP. Oxidative damage and protection of the RPE. Prog Retin Eye Res. 2000; 19 (2): 205-221.
65. Fessel JP, Jackson Roberts L. Isofurans: novel products of lipid peroxidation that define the occurrence of oxidant injury in settings of elevated oxygen tension. Antioxid Redox Signal. 2005; 7 (1-2): 202-209.
66. Burger D, Touyz RM. Cellular biomarkers of endothelial health: microparticles, endothelial progenitor cells, and circulating endothelial cells. J AmSoc Hypertens. 2012; 6 (2): 85-99.
67. Mullins RF, Johnson MN, Faidley EA, Skeie JM, Huang J. Choriocapillaris vascular dropout related to density of drusen in human eyes with early age-related macular degeneration. Invest Ophthalmol Vis Sci. 2011; 52 (3): 1606-1612.
68. Grossniklaus HE, Ling JX, Wallace TM, et al. Macrophage and retinal pigment epithelium expression of angiogenic cytokines in choroidal neovascularization. Mol Vis. 2002; 8: 119-126.
69. Penfold PL, Killingsworth MC, Sarks SH. Senile macular degeneration: the involvement of immunocompetent cells. Graefes Arch Clin Exp Ophthalmol. 1985; 223 (2): 69-76.
70. Skeie JM, Fingert JH, Russell SR, Stone EM, Mullins RF. Complement component C5a activates ICAM-1 expression on human choroidal endothelial cells. Invest Ophthalmol Vis Sci. 2010; 51 (10): 5336-5342.
71. Jonas JB, Tao Y, Neumaier M, Findeisen P. Monocyte chemoattractant protein 1, intercellular adhesion molecule 1, and vascular cell adhesion molecule 1 in exudative age-related macular degeneration. Arch Ophthalmol. 2010; 128 (10): 1281-1286.
72. Chambless LE, Folsom AR, Sharrett AR, et al. Coronary heart disease risk prediction in the Atherosclerosis Risk in Communities (ARIC) Study. J Clin Epidemiol. 2003; 56 (9): 880-890.
73. Folsom AR, Chambless LE, Ballantyne CM, et al. An assessment of incremental coronary risk prediction using C-reactive protein and other novel risk markers: the atherosclerosis risk in communities study. Arch Intern Med. 2006; 166 (13): 1368-1373.
74. Pencina MJ, D'Agostino RB Sr, D'Agostino RB Jr, Vasan RS. Evaluating the added predictive ability of a new marker: from area under the ROC curve to reclassification and beyond. Stat Med. 2008; 27 (2): 157-172, discussion 207-212.
75. Nash SD, Cruickshanks KJ, Klein R, et al. Long-term variability of inflammatory markers and associated factors in a population-based cohort. J AmGeriatr Soc. 2013; 61 (8): 1269-1276.
76. Fontes JD, Yamamoto JF, Larson MG, et al. Clinical correlates of change in inflammatory biomarkers: the Framingham Heart Study. Atherosclerosis. 2013; 228 (1): 217-223.
77. Wu T, Rifai N, Roberts LJ II, WillettWC, Rimm EB. Stability of measurements of biomarkers of oxidative stress in blood over 36 hours. Cancer Epidemiol Biomarkers Prev. 2004; 13 (8): 1399-1402.
78. Schwedhelm E, Boger RH. Application of gas chromatography-mass spectrometry for analysis of isoprostanes: their role in cardiovascular disease. Clin Chem Lab Med. 2003; 41 (12): 1552-1561.