Regression of Some High-risk Features of Age-related Macular Degeneration (AMD) in Patients Receiving Intensive Statin Treatment

EBioMedicine

Volumn 5, Issue , 2016, Pages 198-203

  Vavvas, Demetrios G ^a,b   Daniels, Anthony B ^a,b   Kapsala, Zoi G ^a,b   Goldfarb, Jeremy W ^a,b   Ganotakis, Emmanuel ^a,b   Loewenstein, John I ^a,b   Young, Lucy H ^a,b   Gragoudas, Evangelos S ^a,b   Eliott, Dean ^a,b   Kim, Ivana K ^a,b   Tsilimbaris, Miltiadis K ^a,b   Miller, Joan W ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CRETE   (Greece)

Author keywords

AMD; High dose; Reversal; Soft drusen; Statins; Vision gain

Indexed keywords

ATORVASTATIN;

ADULT; AGE RELATED MACULAR DEGENERATION; ARTICLE; ATHEROSCLEROTIC PLAQUE; CLINICAL ARTICLE; DRUSEN; FUNDUS CAMERA; HUMAN; INTERVENTION STUDY; MALE; MIDDLE AGED; MULTICENTER STUDY; OPEN STUDY; OPTICAL COHERENCE TOMOGRAPHY; PRIORITY JOURNAL; PROSPECTIVE STUDY; RETINA DETACHMENT; VISUAL ACUITY; AGED; ATHEROSCLEROSIS; BLOOD; CLINICAL TRIAL; DRUG EFFECT; FEMALE; MACULAR DEGENERATION; PATHOLOGY; PREGNANCY; RETINAL PIGMENT EPITHELIUM; RISK FACTOR;

AGED; ATHEROSCLEROSIS; ATORVASTATIN; FEMALE; HUMANS; MACULAR DEGENERATION; MALE; MIDDLE AGED; PREGNANCY; PROSPECTIVE STUDIES; RETINAL DETACHMENT; RETINAL DRUSEN; RETINAL PIGMENT EPITHELIUM; RISK FACTORS; TOMOGRAPHY, OPTICAL COHERENCE; VISUAL ACUITY;

EID: 84957899790     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2016.01.033     Document Type: Article

References (74)

1. Arad Y., Ramakrishnan R., Ginsberg H.N. Lovastatin therapy reduces low density lipoprotein apoB levels in subjects with combined hyperlipidemia by reducing the production of apoB-containing lipoproteins: implications for the pathophysiology of apoB production. J. Lipid Res. 1990, 31:567-582.
2. Barathi V.A., Yeo S.W., Guymer R.H., Wong T.Y., Luu C.D. Effects of simvastatin on retinal structure and function of a high-fat atherogenic mouse model of thickened Bruch's membrane. Invest. Ophthalmol. Vis. Sci. 2014, 55:460-468.
3. Bilheimer D.W., Grundy S.M., Brown M.S., Goldstein J.L. Mevinolin and colestipol stimulate receptor-mediated clearance of low density lipoprotein from plasma in familial hypercholesterolemia heterozygotes. Proc. Natl. Acad. Sci. U. S. A. 1983, 80:4124-4128.
4. Brader H.S., Ying G.S., Martin E.R., Maguire M.G. Complications of age-related macular degeneration prevention trial research Group. Characteristics of incident geographic atrophy in the complications of age-related macular degeneration prevention trial. Ophthalmology 2013, 120:1871-1879.
5. Cankova Z., Huang J.D., Kruth H.S., Johnson M. Passage of low-density lipoproteins through Bruch's membrane and choroid. Exp. Eye Res. 2011, 93:947-955.
6. Cannon C.P., Braunwald E., McCabe C.H., et al. Intensive versus moderate lipid lowering with statins after acute coronary syndromes. N. Engl. J. Med. 2004, 350:1495-1504.
7. Chen W., Stambolian D., Edwards A.O., et al. Genetic variants near TIMP3 and high-density lipoprotein-associated loci influence susceptibility to age-related macular degeneration. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7401-7406.
8. Cheng C.Y., Yamashiro K., Chen L.J., et al. New loci and coding variants confer risk for age-related macular degeneration in East Asians. Nat. Commun. 2015, 6:6063.
9. Chitose T., Sugiyama S., Sakamoto K., et al. Effect of a hydrophilic and a hydrophobic statin on cardiac salvage after ST-elevated acute myocardial infarction - a pilot study. Atherosclerosis 2014, 237:251-258.
10. Cougnard-Gregoire A., Delyfer M.N., Korobelnik J.F., et al. Elevated high-density lipoprotein cholesterol and age-related macular degeneration: the Alienor study. PLoS One 2014, 9:e90973.
11. Crabb J.W. The proteomics of drusen. Cold Spring Harb. Perspect. Med. 2014, 4:a017194.
12. Crabb J.W., Miyagi M., Gu X., et al. Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:14682-14687.
13. Curcio C.A., Millican C.L., Bailey T., Kruth H.S. Accumulation of cholesterol with age in human Bruch's membrane. Invest. Ophthalmol. Vis. Sci. 2001, 42:265-274.
14. Curcio C.A., Johnson M., Rudolf M., Huang J.D. The oil spill in ageing Bruch membrane. Br. J. Ophthalmol. 2011, 95:1638-1645.
15. Ethier C.R., Johnson M., Ruberti J. Ocular biomechanics and biotransport. Annu. Rev. Biomed. Eng. 2004, 6:249-273.
16. Fong C.W. Statins in therapy: understanding their hydrophilicity, lipophilicity, binding to 3-hydroxy-3-methylglutaryl-CoA reductase, ability to cross the blood brain barrier and metabolic stability based on electrostatic molecular orbital studies. Eur. J. Med. Chem. 2014, 85:661-674.
17. Friberg T.R., Musch D.C., Lim J.I., et al. Prophylactic treatment of age-related macular degeneration report number 1: 810-nanometer laser to eyes with drusen. Unilaterally eligible patients. Ophthalmology 2006, 113:622 e1.
18. Friedman E., Kopald H.H., Smith T.R. Retinal and choroidal blood flow determined with Krypton-85 anesthetized animals. Invest. Ophthalmol. 1964, 3:539-547.
19. Fritsche L.G., Chen W., Schu M., et al. Seven new loci associated with age-related macular degeneration. Nat. Genet. 2013, 45:433-439. (9e1-2).
20. Fritsche L.G., Igl W., JN Bailey, et al. A large genome-wide association study of age-related macular degeneration highlights contributions of rare and common variants. Nat. Genet. 2015.
21. Garcia Filho C.A., Yehoshua Z., Gregori G., et al. Change in drusen volume as a novel clinical trial endpoint for the study of complement inhibition in age-related macular degeneration. Ophthalmic Surg. Lasers Imaging Retina 2014, 45:18-31.
22. Gehlbach P., Li T., Hatef E. Statins for age-related macular degeneration. Cochrane Database Syst. Rev. 2009, CD006927.
23. Gehlbach P., Li T., Hatef E. Statins for age-related macular degeneration. Cochrane Database Syst. Rev. 2015, 2:CD006927.
24. Guymer R.H., Baird P.N., Varsamidis M., et al. Proof of concept, randomized, placebo-controlled study of the effect of simvastatin on the course of age-related macular degeneration. PLoS One 2013, 8:e83759.
25. Hall N.F., Gale C.R., Syddall H., Phillips D.I., Martyn C.N. Risk of macular degeneration in users of statins: cross sectional study. BMJ 2001, 323:375-376.
26. Hollyfield J.G. 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, 51:1275-1281.
27. Hussain A.A., Starita C., Hodgetts A., Marshall J. Macromolecular diffusion characteristics of ageing human Bruch's membrane: implications for age-related macular degeneration (AMD). Exp. Eye Res. 2010, 90:703-710.
28. Ito T., Ikeda U., Shimpo M., et al. HMG-CoA reductase inhibitors reduce interleukin-6 synthesis in human vascular smooth muscle cells. Cardiovasc. Drugs Ther. 2002, 16:121-126.
29. Johnson L.V., Forest D.L., Banna C.D., et al. Cell culture model that mimics drusen formation and triggers complement activation associated with age-related macular degeneration. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:18277-18282.
30. Khush K.K., Waters D. Lessons from the PROVE-IT trial. higher dose of potent statin better for high-risk patients. Cleve. Clin. J. Med. 2004, 71:609-616.
31. Kim K.J., Kim K.S., Kim N.R., Chin H.S. Effects of simvastatin on the expression of heme oxygenase-1 in human RPE cells. Invest. Ophthalmol. Vis. Sci. 2012, 53:6456-6464.
32. Kino T., Kozasa T., Chrousos G.P. Statin-induced blockade of prenylation alters nucleocytoplasmic shuttling of GTP-binding proteins gamma2 and beta2 and enhances their suppressive effect on glucocorticoid receptor transcriptional activity. Eur. J. Clin. Invest. 2005, 35:508-513.
33. Klein R., Peto T., Bird A., Vannewkirk M.R. The epidemiology of age-related macular degeneration. Am. J. Ophthalmol. 2004, 137:486-495.
34. Klein R., Deng Y., Klein B.E., et al. Cardiovascular disease, its risk factors and treatment, and age-related macular degeneration: women's health initiative sight exam ancillary study. Am. J. Ophthalmol. 2007, 143:473-483.
35. Klein R., Myers C.E., Buitendijk G.H., et al. Lipids, lipid genes, and incident age-related macular degeneration: the three continent age-related macular degeneration consortium. Am. J. Ophthalmol. 2014, 158:513-524. e3.
36. Klein R., Myers C.E., Cruickshanks K.J., et al. 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 Ophthalmol. 2014, 132:446-455.
37. Kramer C.M., Mani V., Fayad Z.A. MR imaging-verified plaque delipidation with lipid-lowering therapy important questions remain. JACC Cardiovasc. Imaging 2011, 4:987-989.
38. Linsenmeier R.A., Braun R.D. Oxygen distribution and consumption in the cat retina during normoxia and hypoxemia. J. Gen. Physiol. 1992, 99:177-197.
39. Luibl V., Isas J.M., Kayed R., Glabe C.G., Langen R., Chen J. Drusen deposits associated with aging and age-related macular degeneration contain nonfibrillar amyloid oligomers. J. Clin. Invest. 2006, 116:378-385.
40. Miller J.W. Age-related macular degeneration revisited-piecing the puzzle: the LXIX Edward Jackson memorial lecture. Am. J. Ophthalmol. 2013, 155:1-35 e13.
41. Moore D.J., Hussain A.A., Marshall J. Age-related variation in the hydraulic conductivity of Bruch's membrane. Invest. Ophthalmol. Vis. Sci. 1995, 36:1290-1297.
42. Mullins R.F., Russell S.R., Anderson D.H., Hageman G.S. Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease. FASEB J. 2000, 14:835-846.
43. Neale B.M., Fagerness J., Reynolds R., et al. Genome-wide association study of advanced age-related macular degeneration identifies a role of the hepatic lipase gene (LIPC). Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7395-7400.
44. Nicholls S.J., Ballantyne C.M., Barter P.J., et al. Effect of two intensive statin regimens on progression of coronary disease. N. Engl. J. Med. 2011, 365:2078-2087.
45. Nissen S.E. Effect of intensive lipid lowering on progression of coronary atherosclerosis: evidence for an early benefit from the reversal of atherosclerosis with aggressive lipid lowering (REVERSAL) trial. Am. J. Cardiol. 2005, 96:61F-68F.
46. Nissen S.E., Tuzcu E.M., Schoenhagen P., et al. Effect of intensive compared with moderate lipid-lowering therapy on progression of coronary atherosclerosis: a randomized controlled trial. JAMA 2004, 291:1071-1080.
47. Nissen S.E., Nicholls S.J., Sipahi I., et al. Effect of very high-intensity statin therapy on regression of coronary atherosclerosis: the ASTEROID trial. JAMA 2006, 295:1556-1565.
48. Pauleikhoff D., Harper C.A., Marshall J., Bird A.C. Aging changes in Bruch's membrane. A histochemical and morphologic study. Ophthalmology 1990, 97:171-178.
49. Pikuleva I.A., Curcio C.A. Cholesterol in the retina: the best is yet to come. Prog. Retin. Eye Res. 2014, 41:64-89.
50. Pitt B., Waters D., Brown W.V., et al. Aggressive lipid-lowering therapy compared with angioplasty in stable coronary artery disease. Atorvastatin versus revascularization treatment investigators. N. Engl. J. Med. 1999, 341:70-76.
51. Profumo E., Buttari B., Saso L., Rigano R. Pleiotropic effects of statins in atherosclerotic disease: focus on the antioxidant activity of atorvastatin. Curr. Top. Med. Chem. 2014, 14:2542-2551.
52. Qian J., Keyes K.T., Long B., Chen G., Ye Y. Impact of HMG-CoA reductase inhibition on oxidant-induced injury in human retinal pigment epithelium cells. J. Cell. Biochem. 2011, 112:2480-2489.
53. Reynolds R., Rosner B., Seddon J.M. Serum lipid biomarkers and hepatic lipase gene associations with age-related macular degeneration. Ophthalmology 2010, 117:1989-1995.
54. Robinson R., Ho C.E., Tan Q.S., et al. Fluvastatin downregulates VEGF-A expression in TNF-alpha-induced retinal vessel tortuosity. Invest. Ophthalmol. Vis. Sci. 2011, 52:7423-7431.
55. Rodriguez I.R., Clark M.E., Lee J.W., Curcio C.A. 7-Ketocholesterol accumulates in ocular tissues as a consequence of aging and is present in high levels in drusen. Exp. Eye Res. 2014, 128:151-155.
56. Sarks J.P., Sarks S.H., Killingsworth M.C. Evolution of soft drusen in age-related macular degeneration. Eye (Lond.) 1994, 8(Pt 3):269-283.
57. Sene A., Apte R.S. Eyeballing cholesterol efflux and macrophage function in disease pathogenesis. Trends Endocrinol. Metab. 2014, 25:107-114.
58. Sene A., Khan A.A., Cox D., et al. Impaired cholesterol efflux in senescent macrophages promotes age-related macular degeneration. Cell Metab. 2013, 17:549-561.
59. Sene A., Chin-Yee D., Apte R.S. Seeing through VEGF: innate and adaptive immunity in pathological angiogenesis in the eye. Trends Mol. Med. 2015, 21:43-51.
60. Sivaprasad S., Bailey T.A., Chong V.N. Bruch's membrane and the vascular intima: is there a common basis for age-related changes and disease?. Clin. Experiment. Ophthalmol. 2005, 33:518-523.
61. 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, 13:772-778.
62. Suzuki M., Tsujikawa M., Itabe H., et al. Chronic photo-oxidative stress and subsequent MCP-1 activation as causative factors for age-related macular degeneration. J. Cell Sci. 2012, 125:2407-2415.
63. Tan J.S., Mitchell P., Rochtchina E., Wang J.J. Statins and the long-term risk of incident age-related macular degeneration: the Blue Mountains eye study. Am. J. Ophthalmol. 2007, 143:685-687.
64. Tomany S.C., Wang J.J., Van Leeuwen R., et al. Risk factors for incident age-related macular degeneration: pooled findings from 3 continents. Ophthalmology 2004, 111:1280-1287.
65. VanderBeek B.L., Zacks D.N., Talwar N., Nan B., Stein J.D. Role of statins in the development and progression of age-related macular degeneration. Retina 2013, 33:414-422.
66. Wang L., Li C.M., Rudolf M., et al. Lipoprotein particles of intraocular origin in human Bruch membrane: an unusual lipid profile. Invest. Ophthalmol. Vis. Sci. 2009, 50:870-877.
67. Winkler B.S., Boulton M.E., Gottsch J.D., Sternberg P. Oxidative damage and age-related macular degeneration. Mol. Vis. 1999, 5:32.
68. Wong W.L., Su X., Li X., et al. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: a systematic review and meta-analysis. Lancet Glob. Health 2014, 2:e106-e116.
69. Wu T., Fujihara M., Tian J., et al. Apolipoprotein B100 secretion by cultured ARPE-19 cells is modulated by alteration of cholesterol levels. J. Neurochem. 2010, 114:1734-1744.
70. Yamada K., Sakurai E., Itaya M., Yamasaki S., Ogura Y. Inhibition of laser-induced choroidal neovascularization by atorvastatin by downregulation of monocyte chemotactic protein-1 synthesis in mice. Invest. Ophthalmol. Vis. Sci. 2007, 48:1839-1843.
71. Yehoshua Z., Wang F., Rosenfeld P.J., Penha F.M., Feuer W.J., Gregori G. Natural history of drusen morphology in age-related macular degeneration using spectral domain optical coherence tomography. Ophthalmology 2011, 118:2434-2441.
72. Yip J.L., Khawaja A.P., Chan M.P., et al. Cross sectional and longitudinal associations between cardiovascular risk factors and age related macular degeneration in the EPIC-Norfolk eye study. PLoS One 2015, 10:e0132565.
73. Yu C.M., Zhang Q., Lam L., et al. Comparison of intensive and low-dose atorvastatin therapy in the reduction of carotid intimal-medial thickness in patients with coronary heart disease. Heart 2007, 93:933-939.
74. Zhao X.Q., Dong L., Hatsukami T., et al. MR imaging of carotid plaque composition during lipid-lowering therapy a prospective assessment of effect and time course. JACC Cardiovasc. Imaging 2011, 4:977-986.