Alzheimer’s disease and the early signs of age-related macular degeneration

Current Alzheimer Research

Volumn 13, Issue 11, 2016, Pages 1259-1266

  Frost, Shaun ^a   Guymer, Robyn ^b   Aung, Khin Zaw ^b   Macaulay, S Lance ^a   Sohrabi, Hamid R ^c   Bourgeat, Pierrick ^a   Salvado, Olivier ^a   Rowe, Christopher C ^d   Ames, David ^e   Masters, Colin L ^f   Martins, Ralph N ^c   Kanagasingam, Yogesan ^a   Aibl Research Group, ^g  

^a CSIRO   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c EDITH COWAN UNIVERSITY   (Australia)

^d AUSTIN HEALTH   (Australia)

^e NATIONAL AGEING RESEARCH INSTITUTE   (Australia)

^f FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^g AIBL   (Australia)

Author keywords

Aging; Alzheimer s; Diagnosis; Eye; Retina; Vision disorders

Indexed keywords

APOENZYME; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; APOLIPOPROTEIN E;

AGE; AGE RELATED MACULAR DEGENERATION; AGED; ALZHEIMER DISEASE; ARTICLE; CATARACT EXTRACTION; CLINICAL ARTICLE; CLINICAL FEATURE; COHORT ANALYSIS; COMORBIDITY; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HUMAN; HYPERTENSION; MALE; NEUROIMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RISK FACTOR; SMOKING; ANALYSIS OF VARIANCE; AUSTRALIA; COMPLICATION; DIAGNOSTIC IMAGING; GENETICS; MACULAR DEGENERATION; MIDDLE AGED; PATHOLOGY; RETINA; STATISTICAL MODEL; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANALYSIS OF VARIANCE; APOLIPOPROTEINS E; AUSTRALIA; COHORT STUDIES; FEMALE; HUMANS; LOGISTIC MODELS; MACULAR DEGENERATION; MALE; MIDDLE AGED; NEUROIMAGING; RETINA;

EID: 84995769913     PISSN: 15672050     EISSN: 18755828     Source Type: Journal    
DOI: 10.2174/1567205013666160603003800     Document Type: Article

References (94)

1. Klein R, Peto T, Bird A, Vannewkirk MR. The epidemiology of age-related macular degeneration. Am J Ophthalmol 137: 486-495 (2004).
2. Global Data on Visual Impairments. USA: World Health Organization (2010).
3. Fine SL, Berger JW, Maguire MG, Ho AC. Age-related macular degeneration. N Engl J Med 342: 483-492 (2000).
4. Sparrow JR. Bisretinoids of RPE lipofuscin: trigger for complement activation in age-related macular degeneration. Adv Exp Med Biol 703: 63-74 (2010).
5. Johnson LV, Leitner WP, Rivest AJ, Staples MK, Radeke MJ, Anderson DH. The Alzheimer’s A beta -peptide is deposited at sites of complement activation in pathologic deposits associated with aging and age-related macular degeneration. Proc Natl Acad Sci USA 99: 11830-11835 (2002).
6. Luibl V, Isas JM, Kayed R, Glabe CG, Langen R, Chen J. Drusen deposits associated with aging and age-related macular degeneration contain nonfibrillar amyloid oligomers. J Clin Investig 116: 378-385 (2006).
7. Anderson DH, Talaga KC, Rivest AJ, Barron E, Hageman GS, Johnson LV. Characterization of [beta] amyloid assemblies in drusen: the deposits associated with aging and age-related macular degeneration. Exp Eye Res 78: 243-256 (2004).
8. Dentchev T, Milam AH, Lee VMY, Trojanowski JQ, Dunaief JL. Amyloid-β is found in drusen from some age-related macular degeneration retinas, but not in drusen from normal retinas1 1 Edited by Hans E. Grossniklaus, MD. Am J Ophthalmol 136: 787 (2003).
9. Ohno-Matsui K. Parallel findings in age-related macular degeneration and Alzheimer’s disease. Prog Retin Eye Res 30: 217-238 (2011).
10. Klaver CC, Ott A, Hofman A, Assink JJ, Breteler MM, de Jong PT. Is age-related maculopathy associated with Alzheimer’s Disease? The Rotterdam Study. Am J Epidemiol 150: 963-968 (1999).
11. Hoh Kam J, Lenassi E, Jeffery G, Viewing Ageing Eyes: Diverse Sites of Amyloid Beta Accumulation in the Ageing Mouse Retina and the Up-Regulation of Macrophages. PLoS One 5(10): e13127. (2010).
12. Yoshida T, Ohno-Matsui K, Ichinose S, Sato T, Iwata N, Saido TC, et al. The potential role of amyloid beta in the pathogenesis of agerelated macular degeneration. J Clin Invest 115: 2793-2800 (2005).
13. Ravona-Springer R, Davidson M, Noy S. The role of cardiovascular risk factors in Alzheimer’s disease. CNS Spectr 8: 824-833 (2003).
14. Thal DR, Ghebremedhin E, Orantes M, Wiestler OD. Vascular pathology in Alzheimer disease: correlation of cerebral amyloid angiopathy and arteriosclerosis/lipohyalinosis with cognitive decline. J Neuropathol Exp Neurol 62: 1287-1301 (2003).
15. de la Torre JC. Cerebrovascular and cardiovascular pathology in Alzheimer’s disease. Int Rev Neurobiol 84: 35-48 (2009).
16. Ruitenberg A, den Heijer T, Bakker SL, van Swieten JC, Koudstaal PJ, Hofman A, et al. Cerebral hypoperfusion and clinical onset of dementia: the Rotterdam Study. Ann Neurol 57: 789-794 (2005).
17. Guymer R, Cipriani T, Rittenhouse KD, Lim L, Robman LD, Li W, et al. Plasma levels of amyloid beta and other proinflammatory mediators in patients with age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol 253: 1347-1354 (2015).
18. Lui JK, Laws SM, Li QX, Villemagne VL, Ames D, Brown B, et al. Plasma amyloid-beta as a biomarker in Alzheimer’s disease: the AIBL study of aging. J Alzheimers Dis 20: 1233-1242 (2010)
19. Berisha F, Feke GT, Trempe CL, McMeel JW, Schepens CL. Retinal abnormalities in early Alzheimer’s disease. Invest Ophthalmol Vis Sci 48:, 2285-2289 (2007).
20. Tsai CS. Optic nerve head and nerve fiber layer in Alzheimer’s disease. Arch Ophthalmol 109: 199 (1991).
21. Danesh-Meyer HV, Birch H, Ku JY, Carroll S, Gamble G. Reduction of optic nerve fibers in patients with Alzheimer disease identified by laser imaging. Neurology 67: 1852-1854 (2006).
22. Bayer AU, Ferrari F, Erb C. High Occurrence Rate of Glaucoma among Patients with Alzheimer’s Disease. Eur Neurol 47: 165-168 (2002).
23. Tamura H, Kawakami H, Kanamoto T, Kato T, Yokoyama T, Sasaki K, et al. High frequency of open-angle glaucoma in Japanese patients with Alzheimer’s disease. J Neurol Sci 246: 79-83 (2006).
24. Blanks JC, Hinton DR, Sadun AA, Miller CA. Retinal ganglion cell degeneration in Alzheimer’s disease. Brain Res 501: 364-372 (1989).
25. Blanks JC, Schmidt SY, Torigoe Y, Porrello KV, Hinton DR, Blanks RH. Retinal pathology in Alzheimer’s disease. II. Regional neuron loss and glial changes in GCL. Neurobiol Aging 17: 385-395 (1996).
26. Blanks JC, Torigoe Y, Hinton DR, Blanks RH. Retinal pathology in Alzheimer’s disease. I. Ganglion cell loss in foveal/parafoveal retina. Neurobiol Aging 17: 377-384 (1996).
27. Hinton DR, Sadun AA, Blanks JC, Miller CA. Optic-nerve degeneration in Alzheimer’s disease. N Engl J Med 315: 485-487 (1986).
28. Sadun AA, Bassi CJ. The visual system in Alzheimer’s disease. Res Publ Assoc Res Nerv Ment Dis 67: 331-347 (1990).
29. Sadun AA, Bassi CJ. Optic nerve damage in Alzheimer’s disease. Ophthalmology 97: 9-17 (1990).
30. Paquet C, Boissonnot M, Roger F, Dighiero P, Gil R, Hugon J. Abnormal retinal thickness in patients with mild cognitive impairment and Alzheimer’s disease. Neurosci Lett 420: 97-99 (2007).
31. Parisi V, Restuccia R, Fattapposta F, Mina C, Bucci MG, Pierelli F. Morphological and functional retinal impairment in Alzheimer’s disease patients. Clin Neurophysiol 112: 1860-1867 (2001).
32. Iseri PK, Altinas O, Tokay T, Yuksel N. Relationship between cognitive impairment and retinal morphological and visual functional abnormalities in Alzheimer disease. J Neuroophthalmol 26: 18-24 (2006).
33. Frost S, Kanagasingam Y, Sohrabi H, Vignarajan J, Bourgeat P, Salvado O, et al. Retinal vascular biomarkers for early detection and monitoring of Alzheimer’s disease. Transl Psychiatry 3: e233 (2013a).
34. Koronyo-Hamaoui M, Koronyo Y, Ljubimov AV, Miller CA, Ko MK, Black KL, et al. Identification of amyloid plaques in retinas from Alzheimer’s patients and noninvasive in vivo optical imaging of retinal plaques in a mouse model. Neuroimage 54: S204-217 (2011).
35. Koronyo Y, Salumbides BC, Black KL, Koronyo-Hamaoui M. Alzheimer’s disease in the retina: imaging retinal abeta plaques for early diagnosis and therapy assessment. Neurodegener Dis 10: 285- 293 (2012).
36. Kaarniranta K, Salminen A, Haapasalo A, Soininen H, Hiltunen M. Age-related macular degeneration (AMD): Alzheimer’s disease in the eye? J Alzheimers Dis 24: 615-631 (2011).
37. Chakravarthy U, Wong TY, Fletcher A, Piault E, Evans C, Zlateva G, et al. Clinical risk factors for age-related macular degeneration: a systematic review and meta-analysis. BMC Ophthalmol 10: 31 (2010).
38. Rosendorff C, Beeri MS, Silverman JM. Cardiovascular risk factors for Alzheimer’s disease. Am J Geriatr Cardiol 16: 143-149 (2007).
39. Klaver CC, Kliffen M, van Duijn CM, Hofman A, Cruts M, Grobbee DE, et al. Genetic association of apolipoprotein E with agerelated macular degeneration. Am J Hum Genet 63: 200-206 (1998).
40. Souied EH, Benlian P, Amouyel P, Feingold J, Lagarde JP, Munnich A, et al. The epsilon4 allele of the apolipoprotein E gene as a potential protective factor for exudative age-related macular degeneration. Am J Ophthalmol 125: 353-359 (1998).
41. Kim J, Basak JM, Holtzman DM. The role of apolipoprotein E in Alzheimer’s disease. Neuron 63: 287-303 (2009).
42. Smith JD. Apolipoprotein E4: an allele associated with many diseases. Ann Med 32: 118-127 (2000).
43. Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C, et al. American Heart Association Stroke Council CoE, Prevention CoCNCoCR, Intervention, Council on Cardiovascular S, Anesthesia. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the american heart association/american stroke association. Stroke 42: 2672-2713 (2011).
44. Knopman DS. Cerebrovascular pathology in cognitive impairment: new (in)sights. Neurology 78: 1032-1033 (2012).
45. Knopman DS. Cerebrovascular disease and dementia. Br J Radiol 80 (Spec No 2): S121-127 (2007).
46. Baird PN, Guida E, Chu DT, Vu HT, Guymer RH. The epsilon2 and epsilon4 alleles of the apolipoprotein gene are associated with age-related macular degeneration. Invest Ophthalmol Vis Sci 45: 1311-1315 (2004).
47. Schmidt S, Klaver C, Saunders A, Postel E, De La Paz M, Agarwal A, et al. A pooled case-control study of the apolipoprotein E (APOE) gene in age-related maculopathy. Ophthalmic Genet 23: 209-223 (2002).
48. Zareparsi S, Reddick AC, Branham KE, Moore KB, Jessup L, Thoms S, et al. Association of apolipoprotein E alleles with susceptibility to age-related macular degeneration in a large cohort from a single center. Invest Ophthalmol Vis Sci 45: 1306-1310 (2004).
49. Wong TY, Shankar A, Klein R, Bray MS, Couper DJ, Klein BE, et al. Apolipoprotein E gene and early age-related maculopathy: the Atherosclerosis Risk in Communities Study. Ophthalmology 113: 255-259 (2006).
50. Baker ML, Wang JJ, Rogers S, Klein R, Kuller LH, Larsen EK, et al. Early age-related macular degeneration, cognitive function, and dementia: the Cardiovascular Health Study. Arch Ophthalmol 127: 667-673 (2009).
51. Williams MA, Silvestri V, Craig D, Passmore AP, Silvestri G. The prevalence of age-related macular degeneration in Alzheimer’s disease. J Alzheimers Dis 42: 909-914 (2014).
52. Keenan TD, Goldacre R, Goldacre MJ. Associations between agerelated macular degeneration, Alzheimer disease, and dementia: record linkage study of hospital admissions. JAMA Ophthalmol 132: 63-68 (2014).
53. Pham TQ, Kifley A, Mitchell P, Wang JJ. Relation of age-related macular degeneration and cognitive impairment in an older population. Gerontology 52: 353-358 (2006).
54. Rozzini L, Riva M, Ghilardi N, Facchinetti P, Forbice E, Semeraro F, et al. Cognitive dysfunction and age-related macular degeneration. Am J Alzheimers Dis Other Dement 29: 256-262 (2014).
55. Ding J, Patton N, Deary IJ, Strachan MW, Fowkes FG, Mitchell RJ, et al. Retinal microvascular abnormalities and cognitive dysfunction: a systematic review. Br J Ophthalmol 92: 1017-1025 (2008).
56. Woo SJ, Park KH, Ahn J, Choe JY, Jeong H, Han JW, et al. Cognitive impairment in age-related macular degeneration and geographic atrophy. Ophthalmology 119: 2094-2101 (2012).
57. Cai J, Qi X, Kociok N, Skosyrski S, Emilio A, Ruan Q, et al. beta- Secretase (BACE1) inhibition causes retinal pathology by vascular dysregulation and accumulation of age pigment. EMBO Mol Med 4: 980-991 (2012).
58. Ding JD, Johnson LV, Herrmann R, Farsiu S, Smith SG, Groelle M, et al. Anti-amyloid therapy protects against retinal pigmented epithelium damage and vision loss in a model of age-related macular degeneration. Proc Natl Acad Sci USA 108: E279-287 (2011).
59. Ding JD, Lin J, Mace BE, Herrmann R, Sullivan P, Bowes Rickman C. Targeting age-related macular degeneration with Alzheimer’s disease based immunotherapies: anti-amyloid-beta antibody attenuates pathologies in an age-related macular degeneration mouse model. Vision Res 48: 339-345 (2008).
60. Fagan AM, Mintun MA, Mach RH, Lee SY, Dence CS, Shah AR, et al. Inverse relation between in vivo amyloid imaging load and cerebrospinal fluid Abeta42 in humans. Ann Neurol 59: 512-519 (2006).
61. Morris JC, Roe CM, Grant EA, Head D, Storandt M, Goate AM, et al. Pittsburgh compound B imaging and prediction of progression from cognitive normality to symptomatic Alzheimer disease. Arch Neurol 66: 1469-1475 (2009).
62. Rowe CC, Ellis KA, Rimajova M, Bourgeat P, Pike KE, Jones G, et al. Amyloid imaging results from the Australian Imaging, Biomarkers and Lifestyle (AIBL) study of aging. Neurobiol Aging 31: 1275-1283 (2010).
63. Thal LJ, Kantarci K, Reiman EM, Klunk WE, Weiner MW, Zetterberg H, et al. The role of biomarkers in clinical trials for Alzheimer disease. Alzheimer Dis Assoc Disord 20: 6-15 (2006).
64. Okello A, Koivunen J, Edison P, Archer HA, Turkheimer FE, Nagren K, et al. Conversion of amyloid positive and negative MCI to AD over 3 years: an 11C-PIB PET study. Neurology 73: 754-760 (2009).
65. Pike KE, Savage G, Villemagne VL, Ng S, Moss SA, Maruff P, et al. Beta-amyloid imaging and memory in non-demented individuals: evidence for preclinical Alzheimer’s disease. Brain 130: 2837-2844 (2007).
66. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, et al. Toward defining the preclinical stages of Alzheimer’s disease: recommendations from the National Institute on Aging- Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7: 280-292 (2011).
67. Ellis KA, Bush AI, Darby D, De Fazio D, Foster J, Hudson P, et al. The Australian Imaging, Biomarkers and Lifestyle (AIBL) study of aging: methodology and baseline characteristics of 1112 individuals recruited for a longitudinal study of Alzheimer’s disease. Int Psychogeriatry 21: 672-687 (2009).
68. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology 34: 939-944 (1984).
69. Ingelsson M, Shin Y, Irizarry MC, Hyman BT, Lilius L, Forsell C, et al. Genotyping of apolipoprotein e: comparative evaluation of different protocols. In: Current Protocols in Human Genetics. USA: John Wiley & Sons, Inc. (2003).
70. Hixson JE, Vernier DT. Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J Lipid Res 31: 545-548 (1990).
71. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12: 189-198 (1975).
72. Ferris FL, 3rd, Wilkinson CP, Bird A, Chakravarthy U, Chew E, Csaky K, et al. Clinical classification of age-related macular degeneration. Ophthalmology 120: 844-851 (2013).
73. Chong EW, Wang Y, Robman LD, Aung KZ, Makeyeva GA, Giles GG, et al. Age related macular degeneration and total hip replacement due to osteoarthritis or fracture: melbourne collaborative cohort study. PLoS One 10: e0137322 (2015).
74. Bourgeat P, Chetelat G, Villemagne VL, Fripp J, Raniga P, Pike K, et al. Beta-amyloid burden in the temporal neocortex is related to hippocampal atrophy in elderly subjects without dementia. Neurology 74: 121-127 (2010).
75. Bateman RJ, Xiong C, Benzinger TL, Fagan AM, Goate A, Fox NC, et al. Clinical and Biomarker Changes in Dominantly Inherited Alzheimer’s Disease. N Engl J Med 367: 795-804 (2012).
76. Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, Holt DP, et al. Imaging brain amyloid in Alzheimer’s disease with Pittsburgh Compound-B. Ann Neurol 55: 306-319 (2004).
77. Klunk WE, Lopresti BJ, Ikonomovic MD, Lefterov IM, Koldamova RP, Abrahamson EE, et al. Binding of the positron emission tomography tracer Pittsburgh compound-B reflects the amount of amyloid-beta in Alzheimer’s disease brain but not in transgenic mouse brain. J Neurosci 25: 10598-10606 (2005).
78. Villemagne V, Pike K, Fodero-Tavoletti M, Jones G, McLean C, Hinton F. Age dependent prevalence of beta-amyloid positive 11CPiB PET in healthy elderly subjects parallels neuropathology findings. J Nucl Med Meeting Abstracts 49 (5): 34 (2008).
79. Crabb JW, Miyagi M, Gu X, Shadrach K, West KA, Sakaguchi H, et al. Drusen proteome analysis: an approach to the etiology of agerelated macular degeneration. Proc Natl Acad Sci USA 99: 14682-14687 (2002).
80. Buschini E, Piras A, Nuzzi R, Vercelli A. Age related macular degeneration and drusen: neuroinflammation in the retina. Prog Neurobiol 95: 14-25 (2011).
81. van Splunder J, Stilma JS, Bernsen RMD, Evenhuis HM. Prevalence of ocular diagnoses found on screening 1539 adults with intellectual disabilities. Ophthalmology 111: 1457-1463 (2004).
82. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al. Inflammation and Alzheimer’s disease. Neurobiol Aging 21: 383-421 (2000).
83. Chen M, Muckersie E, Forrester JV, Xu H. Immune activation in retinal aging: a gene expression study. Invest Ophthalmol Vis Sci 51: 5888-5896 (2010).
84. Anthony JC, Breitner JC, Zandi PP, Meyer MR, Jurasova I, Norton MC, et al. Reduced prevalence of AD in users of NSAIDs and H2 receptor antagonists: the Cache County study. Neurology 54: 2066-2071 (2000).
85. Breitner JC, Welsh KA, Helms MJ, Gaskell PC, Gau BA, Roses AD, et al. Delayed onset of Alzheimer’s disease with nonsteroidal anti-inflammatory and histamine H2 blocking drugs. Neurobiol Aging 16: 523-530 (1995).
86. Breitner JC, Zandi PP. Do nonsteroidal antiinflammatory drugs reduce the risk of Alzheimer’s disease? N Engl J Med 345: 1567-1568 (2001).
87. in t’ Veld BA, Ruitenberg A, Hofman A, Launer LJ, van Duijn CM, Stijnen T, et al. Nonsteroidal antiinflammatory drugs and the risk of Alzheimer’s disease. N Engl J Med 345: 1515-1521 (2001).
88. McGeer PL, McGeer EG. NSAIDs and Alzheimer disease: epidemiological, animal model and clinical studies. Neurobiol Aging 28: 639-647 (2007).
89. Szekely CA, Thorne JE, Zandi PP, Ek M, Messias E, Breitner JC, et al. Nonsteroidal anti-inflammatory drugs for the prevention of Alzheimer’s disease: a systematic review. Neuroepidemiology 23: 159-169 (2004).
90. Jaturapatporn D, Isaac MG, McCleery J, Tabet N. Aspirin, steroidal and non-steroidal anti-inflammatory drugs for the treatment of Alzheimer’s disease. Cochrane Database Syst Rev 2: CD006378 (2012).
91. Christen WG. Long-term aspirin use and neovascular age-related macular degeneration: association or causation? Evid Based Med 19(1): e6 (2014).
92. Christen WG, Glynn RJ, Chew EY, Buring JE. Low-dose aspirin and medical record-confirmed age-related macular degeneration in a randomized trial of women. Ophthalmology 116: 2386-2392 (2009).
93. Wilson HL, Schwartz DM, Bhatt HR, McCulloch CE, Duncan JL. Statin and aspirin therapy are associated with decreased rates of choroidal neovascularization among patients with age-related macular degeneration. Am J Ophthalmol 137: 615-624 (2004).
94. Hageman GS, Anderson DH, Johnson LV, Hancox LS, Taiber AJ, Hardisty LI, et al. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to agerelated macular degeneration. Proc Natl Acad Sci U S A 102: 7227- 7232 (2005).