Age, sex, and APOE ϵ4 effects on memory, brain structure, and β-Amyloid across the adult life Span

JAMA Neurology

Volumn 72, Issue 5, 2015, Pages 511-519

  Jack, Clifford R ^a   Wiste, Heather J ^a   Weigand, Stephen D ^a   Knopman, David S ^a   Vemuri, Prashanthi ^a   Mielke, Michelle M ^a   Lowe, Val ^a   Senjem, Matthew L ^a   Gunter, Jeffrey L ^a   Machulda, Mary M ^a   Gregg, Brian E ^a   Pankratz, V Shane ^a   Rocca, Walter A ^a   Petersen, Ronald C ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; PITTSBURGH COMPOUND B; APOLIPOPROTEIN E4;

ADULT; AGE; AGED; APOE EPSILON 4 GENE; ARTICLE; BRAIN SIZE; COGNITION; COHORT ANALYSIS; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FEMALE; GENE; HETEROZYGOTE; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LIFESPAN; MALE; MEMORY; NORMAL HUMAN; OBSERVATIONAL STUDY; POPULATION RESEARCH; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SEX; AGING; ANATOMY AND HISTOLOGY; BRAIN; GENETICS; METABOLISM; MIDDLE AGED; PHYSIOLOGY; SEX DIFFERENCE; VERY ELDERLY;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; AGING; AMYLOID BETA-PEPTIDES; APOLIPOPROTEIN E4; BRAIN; CROSS-SECTIONAL STUDIES; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MEMORY; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY; SEX FACTORS;

EID: 84981225490     PISSN: 21686149     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamaneurol.2014.4821     Document Type: Article

References (61)

1. Villemagne VL, Burnham S, Bourgeat P, et al; Australian Imaging Biomarkers and Lifestyle (AIBL) Research Group. Amyloid β deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer's disease: a prospective cohort study. Lancet Neurol. 2013;12(4):357-367.
2. Rodrigue KM, Kennedy KM, Devous MD Sr, et al. β-Amyloid burden in healthy aging: regional distribution and cognitive consequences. Neurology. 2012;78(6):387-395.
3. Johnson SC, Christian BT, Okonkwo OC, et al. Amyloid burden and neural function in people at risk for Alzheimer's disease. Neurobiol Aging.2014; 35(3):576-584.
4. Jack CR Jr, Wiste HJ, Weigand SD, et al. Age-specific population frequencies of cerebral β-amyloidosis and neurodegeneration among people with normal cognitive function aged 50-89 years: a cross-sectional study. Lancet Neurol. 2014;13(10):997-1005.
5. Roberts RO, Geda YE, Knopman DS, et al. The Mayo Clinic Study of Aging: design and sampling, participation, baseline measures and sample characteristics. Neuroepidemiology. 2008;30(1): 58-69.
6. Klunk WE, Engler H, Nordberg A, et al. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann Neurol. 2004;55(3): 306-319.
7. Senjem ML, Gunter JL, Shiung MM, Petersen RC, Jack CR Jr. Comparison of different methodological implementations of voxel-based morphometry in neurodegenerative disease. Neuroimage. 2005;26 (2):600-608.
8. Jack CR Jr, Knopman DS, Weigand SD, et al. An operational approach to NIA-AA crtiteria for preclinical Alzheimer's disease. Ann Neurol.2012;71 (6):765-775.
9. Klunk WE, Koeppe RA, Price JC, et al. The Centiloid Project: standardizing quantitative amyloid plaque estimation by PET. Alzheimers Dement.2015;11(1):1-15.e4.
10. Jack CR Jr, Knopman DS, Jagust WJ, et al. Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol. 2010;9(1):119-128.
11. Harrell FE. Regression Modeling Strategies: With Applications to Linear Models, Logistic Regression, and Survival Analysis. New York, NY: Springer-Verlag; 2001.
12. Jack CR Jr, Wiste HJ, Knopman DS, et al. Rates of β-amyloid accumulation are independent of hippocampal neurodegeneration. Neurology.2014; 82(18):1605-1612.
13. Jack CR Jr, Wiste HJ, Weigand SD, et al. Amyloid-first and neurodegeneration-first profiles characterize incident amyloid PET positivity. Neurology. 2013;81(20):1732-1740.
14. Fleisher AS, Chen K, Liu X, et al. Apolipoprotein E ϵ4 and age effects on florbetapir positron emission tomography in healthy aging and Alzheimer disease.Neurobiol Aging. 2013;34(1):1-12.
15. Mormino EC, Brandel MG, Madison CM, et al. Not quite PIB-positive, not quite PIB-negative: slight PIB elevations in elderly normal control subjects are biologically relevant. Neuroimage. 2012;59(2):1152-1160.
16. Morris JC, Roe CM, Xiong C, et al. APOE predicts amyloid-β but not tau Alzheimer pathology in cognitively normal aging. Ann Neurol. 2010;67(1): 122-131.
17. Vemuri P, Wiste HJ, Weigand SD, et al; Alzheimer's Disease Neuroimaging Initiative. Effect of apolipoprotein E on biomarkers of amyloid load and neuronal pathology in Alzheimer disease. Ann Neurol. 2010;67(3):308-316.
18. Hedden T, Oh H, Younger AP, Patel TA. Meta-analysis of amyloid-cognition relations in cognitively normal older adults. Neurology.2013; 80(14):1341-1348.
19. Doré V, Villemagne VL, Bourgeat P, et al. Cross-sectional and longitudinal analysis of the relationship between Aβ deposition, cortical thickness, and memory in cognitively unimpaired individuals and in Alzheimer disease. JAMA Neurol. 2013;70(7):903-911.
20. Landau SM, Mintun MA, Joshi AD, et al; Alzheimer's Disease Neuroimaging Initiative. Amyloid deposition, hypometabolism, and longitudinal cognitive decline. Ann Neurol. 2012;72 (4):578-586.
21. Rowe CC, Bourgeat P, Ellis KA, et al. Predicting Alzheimer disease with β-amyloid imaging: results from the Australian Imaging, Biomarkers, and Lifestyle Study of Ageing. Ann Neurol. 2013;74(6): 905-913.
22. Lim YY, Pietrzak RH, Bourgeat P, et al. Relationships between performance on the Cogstate Brief Battery, neurodegeneration, and Aβ accumulation in cognitively normal older adults and adults with MCI. Arch Clin Neuropsychol.2015;301 (1):49-58.
23. Chételat G, Villemagne VL, Pike KE, et al; Australian Imaging, Biomarkers, and Lifestyle Study of Ageing Research Group. Relationship between memory performance and β-amyloid deposition at different stages of Alzheimer's disease. Neurodegener Dis. 2012;10(1-4):141-144.
24. Donohue MC, Sperling RA, Salmon DP, et al; Australian Imaging, Biomarkers, and Lifestyle Flagship Study of Ageing; Alzheimer's Disease Neuroimaging Initiative; Alzheimer's Disease Cooperative Study. The Preclinical Alzheimer Cognitive Composite: measuring amyloid-related decline.JAMA Neurol. 2014;71(8):961-970.
25. Van der Elst W, van Boxtel MP, van Breukelen GJ, Jolles J. Rey's Verbal Learning Test: normative data for 1855 healthy participants aged 24-81 years and the influence of age, sex, education, and mode of presentation. J Int Neuropsychol Soc. 2005;11 (3):290-302.
26. Hedden T, Gabrieli JD. Insights into the ageing mind: a view from cognitive neuroscience. Nat Rev Neurosci. 2004;5(2):87-96.
27. DeCarli C, Massaro J, Harvey D, et al. Measures of brain morphology and infarction in the Framingham Heart Study: establishing what is normal.Neurobiol Aging. 2005;26(4):491-510.
28. Raz N, Lindenberger U, Rodrigue KM, et al. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex. 2005;15(11):1676-1689.
29. Benzinger TL, Blazey T, Jack CR Jr, et al. Regional variability of imaging biomarkers in autosomal dominant Alzheimer's disease. Proc Natl Acad SciUSA. 2013;110(47):4502-4509. doi: 10.1073/pnas.1317918110.
30. Jack CR Jr, Wiste HJ, Lesnick TG, et al. Brain β-amyloid load approaches a plateau. Neurology. 2013;80(10):890-896.
31. Jack CR Jr, Vemuri P, Wiste HJ, et al; Alzheimer's Disease Neuroimaging Initiative. Evidence for ordering of Alzheimer disease biomarkers. Arch Neurol. 2011;68(12):1526-1535.
32. Jagust W. Apolipoprotein E, neurodegeneration, and Alzheimer disease. JAMA Neurol.2013; 70(3):299-300.
33. Chételat G. Alzheimer disease: Aβ-independent processes: rethinking preclinical AD. Nat Rev Neurol. 2013;9(3):123-124.
34. Jack CR Jr, Knopman DS, Jagust WJ, et al. Tracking pathophysiological processes in Alzheimer's disease: an updated hypothetical model of dynamic biomarkers. Lancet Neurol.2013; 12(2):207-216.
35. Wirth M, Madison CM, Rabinovici GD, Oh H, Landau SM, Jagust WJ. Alzheimer's disease neurodegenerative biomarkers are associated with decreased cognitive function but not β-amyloid in cognitively normal older individuals. J Neurosci. 2013;33(13):5553-5563.
36. Fjell AM, McEvoy L, Holland D, Dale AM, Walhovd KB; Alzheimer's Disease Neuroimaging Initiative. Brain changes in older adults at very low risk for Alzheimer's disease. J Neurosci. 2013;33(19): 8237-8242.
37. Nebes RD, Snitz BE, Cohen AD, et al. Cognitive aging in persons with minimal amyloid-β and white matter hyperintensities. Neuropsychologia. 2013;51 (11):2202-2209.
38. Price JL, Morris JC. Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann Neurol. 1999;45(3):358-368.
39. Crary JF, Trojanowski JQ, Schneider JA, et al. Primary age-related tauopathy (PART): a common pathology associated with human aging. Acta Neuropathol. 2014;128(6):755-766.
40. Jagust W. Vulnerable neural systems and the borderland of brain aging and neurodegeneration. Neuron. 2013;77(2):219-234.
41. Sperling RA, Aisen PS, Beckett LA, 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. 2011;7(3): 280-292.
42. Duyckaerts C, Hauw JJ. Prevalence, incidence and duration of Braak's stages in the general population: can we know? Neurobiol Aging.1997;18 (4):362-369.
43. Delacourte A, Sergeant N, Wattez A, et al. Tau aggregation in the hippocampal formation: an ageing or a pathological process? Exp Gerontol. 2002;37(10-11):1291-1296.
44. Jack CR Jr, Holtzman DM. Biomarker modeling of Alzheimer's disease. Neuron. 2013;80(6):1347-1358.
45. Musiek ES, Holtzman DM. Origins of Alzheimer's disease: reconciling cerebrospinal fluid biomarker and neuropathology data regarding the temporal sequence of Aβ and tau involvement. Curr Opin Neurol. 2012;25(6):715-720.
46. Storandt M, Head D, Fagan AM, Holtzman DM, Morris JC. Toward a multifactorial model of Alzheimer disease. Neurobiol Aging. 2012;33(10): 2262-2271.
47. Cerhan JR, Folsom AR, Mortimer JA, et al; Atherosclerosis Risk in Communities (ARIC) Study Investigators. Correlates of cognitive function in middle-aged adults. Gerontology. 1998;44(2):95-105.
48. Baron-Cohen S, Knickmeyer RC, Belmonte MK. Sex differences in the brain: implications for explaining autism. Science. 2005;310(5749):819-823.
49. Rocca WA, Bower JH, Maraganore DM, et al. Increased risk of cognitive impairment or dementia in women who underwent oophorectomy before menopause.Neurology. 2007;69(11):1074-1083.
50. Jack CR Jr, Petersen RC, Xu YC, et al. Hippocampal atrophy and apolipoprotein E genotype are independently associated with Alzheimer's disease. Ann Neurol. 1998;43(3):303-310.
51. Protas HD, Chen K, Langbaum JB, et al. Posterior cingulate glucose metabolism, hippocampal glucose metabolism, and hippocampal volume in cognitively normal, late-middle-aged persons at 3 levels of genetic risk for Alzheimer disease. JAMA Neurol. 2013;70(3): 320-325.
52. Reiman EM, Chen K, Alexander GE, et al. Functional brain abnormalities in young adults at genetic risk for late-onset Alzheimer's dementia. Proc Natl Acad SciUSA. 2004;101(1):284-289.
53. Sheline YI, Morris JC, Snyder AZ, et al. APOE4 allele disrupts resting state fMRI connectivity in the absence of amyloid plaques or decreased CSF Aβ42. J Neurosci. 2010;30(50):17035-17040.
54. Filippini N, MacIntosh BJ, Hough MG, et al. Distinct patterns of brain activity in young carriers of theAPOE-ϵ4 allele. Proc Natl Acad SciUSA. 2009;106(17):7209-7214.
55. Caselli RJ, Dueck AC, Osborne D, et al. Longitudinal modeling of age-related memory decline and the APOE ϵ4 effect. N Engl J Med. 2009;361(3):255-263.
56. Shaw P, Lerch JP, Pruessner JC, et al. Cortical morphology in children and adolescents with different apolipoprotein E gene polymorphisms: an observational study. Lancet Neurol. 2007;6(6):494-500.
57. Alexander GE, Bergfield KL, Chen K, et al. Gray matter network associated with risk for Alzheimer's disease in young to middle-aged adults. Neurobiol Aging. 2012;33(12):2723-2732.
58. Jagust WJ, Landau SM; Alzheimer's Disease Neuroimaging Initiative. Apolipoprotein E, not fibrillar β-amyloid, reduces cerebral glucose metabolism in normal aging. J Neurosci.2012;32 (50):18227-18233.
59. Wolf AB, Valla J, Bu G, et al. Apolipoprotein E as a β-amyloid-independent factor in Alzheimer's disease. Alzheimers Res Ther. 2013;5(5):38.
60. Lim YY, Ellis KA, Pietrzak RH, et al; AIBL Research Group. Stronger effect of amyloid load than APOE genotype on cognitive decline in healthy older adults. Neurology. 2012;79(16):1645-1652.
61. Arking RA. Measuring age-related change in individuals. In: Biology of Aging: Observations and Principles. 2nd ed. Sunderland, MA: Sinauer Associates; 1998:61-105.