Early life characteristics and late life burden of cerebral small vessel disease in the Lothian Birth Cohort 1936

Aging

Volumn 8, Issue 9, 2016, Pages 2039-2061

  Field, Thalia S ^a   Doubal, Fergus N ^b   Johnson, Wendy ^c   Backhouse, Ellen ^b   McHutchison, Caroline ^b   Cox, Simon ^b   Corley, Janie ^c   Pattie, Alison ^c   Gow, Alan J ^d   Shenkin, Susan ^c   Cvoro, Vera ^b   Morris, Zoe ^e   Staals, Julie ^f   Bastin, Mark ^b   Deary, Ian J ^c   Wardlaw, Joanna M ^c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d HERIOT WATT UNIVERSITY   (United Kingdom)

^e NHS LOTHIAN   (United Kingdom)

^f MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Aging; Cerebral small vessel disease; MRI; Risk factors; Stroke

Indexed keywords

AGED; BRAIN; CEREBROVASCULAR DISEASE; COGNITION; COHORT ANALYSIS; COST OF ILLNESS; DIAGNOSTIC IMAGING; FEMALE; HUMAN; MALE; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PSYCHOLOGY; RISK FACTOR; SCOTLAND; WHITE MATTER;

AGED; BRAIN; CEREBRAL SMALL VESSEL DISEASES; COGNITION; COHORT STUDIES; COST OF ILLNESS; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; RISK FACTORS; SCOTLAND; WHITE MATTER;

EID: 84991449464     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.101043     Document Type: Article

References (65)

1. Kolominsky-Rabas PL, Weber M, Gefeller O, Neundoerfer B, Heuschmann PU. Epidemiology of ischemic stroke subtypes according to TOAST criteria: incidence, recurrence, and long-term survival in ischemic stroke subtypes: a population-based study. Stroke. 2001; 32:2735-40. doi.org/10.1161/hs1201.100209
2. Sudlow CL, Warlow CP, and International Stroke Incidence Collaboration. Comparable studies of the incidence of stroke and its pathological types: results from an international collaboration. Stroke. 1997; 28:491-99. doi.org/10.1161/01.STR.28.3.491
3. Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C, Launer LJ, Laurent S, Lopez OL, Nyenhuis D, Petersen RC, Schneider JA, Tzourio C, et al, and American Heart Association Stroke Council, Council on Epidemiology and Prevention, Council on Cardiovascular Nursing, Council on Cardiovascular Radiology and Intervention, and Council on Cardiovascular Surgery and Anesthesia. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the american heart association/american stroke association. Stroke. 2011; 42:2672-713. doi.org/10.1161/STR.0b013e3182299496
4. Staals J, Booth T, Morris Z, Bastin ME, Gow AJ, Corley J, Redmond P, Starr JM, Deary IJ, Wardlaw JM. Total MRI load of cerebral small vessel disease and cognitive ability in older people. Neurobiol Aging. 2015; 36:2806-11. doi.org/10.1016/j.neurobiolaging.2015.06.024
5. Schmidt R, Fazekas F, Kapeller P, Schmidt H, Hartung HP. MRI white matter hyperintensities: three-year follow-up of the Austrian Stroke Prevention Study. Neurology. 1999; 53:132-39. doi.org/10.1212/WNL.53.1.132
6. Williams VJ, Leritz EC, Shepel J, McGlinchey RE, Milberg WP, Rudolph JL, Lipsitz LA, Salat DH. Interindividual variation in serum cholesterol is associated with regional white matter tissue integrity in older adults. Hum Brain Mapp. 2013; 34:1826-41. doi.org/10.1002/hbm.22030
7. Gustafson DR, Steen B, Skoog I. Body mass index and white matter lesions in elderly women. An 18-year longitudinal study. Int Psychogeriatr. 2004; 16:327-36 doi.org/10.1017/S1041610204000353
8. Gons RA, van Norden AG, de Laat KF, van Oudheusden LJ, van Uden IW, Zwiers MP, Norris DG, de Leeuw FE. Cigarette smoking is associated with reduced microstructural integrity of cerebral white matter. Brain. 2011; 134:2116-24. doi.org/10.1093/brain/awr145
9. Heye AK, Thrippleton MJ, Chappell FM, Valdés Hernández MC, Armitage PA, Makin SD, Maniega SM, Sakka E, Flatman PW, Dennis MS, Wardlaw JM. Valdes Hernandez MdC, Armitage PA, Makin SD, Maniega SM, Sakka E, Flatman PW, Dennis MS and Wardlaw JM. Blood pressure and sodium: association with MRI markers in cerebral small vessel disease. J Cereb Blood Flow Metab. 2015. doi.org/10.1038/jcbfm.2015.64
10. Wardlaw JM, Allerhand M, Doubal FN, Valdes Hernandez M, Morris Z, Gow AJ, Bastin M, Starr JM, Dennis MS, Deary IJ. Vascular risk factors, large-artery atheroma, and brain white matter hyperintensities. Neurology. 2014; 82:1331-38. doi.org/10.1212/WNL.0000000000000312
11. Deary IJ, Bastin ME, Pattie A, Clayden JD, Whalley LJ, Starr JM, Wardlaw JM. White matter integrity and cognition in childhood and old age. Neurology. 2006; 66:505-12. doi.org/10.1212/01.wnl.0000199954.81900.e2
12. Glymour MM, Tzourio C, Dufouil C. Is cognitive aging predicted by one's own or one's parents' educational level? results from the three-city study. Am J Epidemiol. 2012; 175:750-59. doi.org/10.1093/aje/kwr509
13. Lawlor DA, Batty GD, Clark H, McIntyre S, Leon DA. Association of childhood intelligence with risk of coronary heart disease and stroke: findings from the Aberdeen Children of the 1950s cohort study. Eur J Epidemiol. 2008; 23:695-706. doi.org/10.1007/s10654-008-9281-z
14. Modig Wennerstad K, Silventoinen K, Tynelius P, Bergman L, Rasmussen F. Association between intelligence and type-specific stroke: a populationbased cohort study of early fatal and non-fatal stroke in one million Swedish men. J Epidemiol Community Health. 2010; 64:908-12. doi.org/10.1136/jech.2008.084020
15. McGurn B, Deary IJ, Starr JM. Childhood cognitive ability and risk of late-onset Alzheimer and vascular dementia. Neurology. 2008; 71:1051-56. doi.org/10.1212/01.wnl.0000319692.20283.10
16. Klarenbeek P, van Oostenbrugge RJ, Rouhl RP, Knottnerus IL, Staals J. Ambulatory blood pressure in patients with lacunar stroke: association with total MRI burden of cerebral small vessel disease. Stroke. 2013; 44:2995-99. doi.org/10.1161/STROKEAHA.113.002545
17. Staals J, Makin SD, Doubal FN, Dennis MS, Wardlaw JM. Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology. 2014; 83:1228-34. doi.org/10.1212/WNL.0000000000000837
18. Huijts M, Duits A, van Oostenbrugge RJ, Kroon AA, de Leeuw PW, Staals J. Accumulation of MRI Markers of Cerebral Small Vessel Disease is Associated with Decreased Cognitive Function. A Study in First-Ever Lacunar Stroke and Hypertensive Patients. Front Aging Neurosci. 2013; 5:72. doi.org/10.3389/fnagi.2013.00072
19. Deary IJ, Gow AJ, Taylor MD, Corley J, Brett C, Wilson V, Campbell H, Whalley LJ, Visscher PM, Porteous DJ, Starr JM. The Lothian Birth Cohort 1936: a study to examine influences on cognitive ageing from age 11 to age 70 and beyond. BMC Geriatr. 2007; 7:28. doi.org/10.1186/1471-2318-7-28
20. Booth T, Bastin ME, Penke L, Maniega SM, Murray C, Royle NA, Gow AJ, Corley J, Henderson RD, Hernández MC, Starr JM, Wardlaw JM, Deary IJ. Brain white matter tract integrity and cognitive abilities in community-dwelling older people: the Lothian Birth Cohort, 1936. Neuropsychology. 2013; 27:595-607. doi.org/10.1037/a0033354
21. Deary IJ, Gow AJ, Pattie A, Starr JM. Cohort profile: the Lothian Birth Cohorts of 1921 and 1936. Int J Epidemiol. 2012; 41:1576-84. doi.org/10.1093/ije/dyr197
22. Johnson W, Corley J, Starr JM, Deary IJ. Psychological and physical health at age 70 in the Lothian Birth Cohort 1936: links with early life IQ, SES, and current cognitive function and neighborhood environment. Health Psychol. 2011; 30:1-11. doi.org/10.1037/a0021834
23. Deary IJ, Whiteman MC, Starr JM, Whalley LJ, Fox HC. The impact of childhood intelligence on later life: following up the Scottish mental surveys of 1932 and 1947 J Pers Soc Psychol. 2004; 86:130-47. doi.org/10.1037/0022-3514.86.1.130
24. Wardlaw JM, Bastin ME, Valdés Hernández MC, Maniega SM, Royle NA, Morris Z, Clayden JD, Sandeman EM, Eadie E, Murray C, Starr JM, Deary IJ. Brain aging, cognition in youth and old age and vascular disease in the Lothian Birth Cohort 1936: rationale, design and methodology of the imaging protocol. Int J Stroke. 2011; 6:547-59. doi.org/10.1111/j.1747-4949.2011.00683.x
25. Cordonnier C, Potter GM, Jackson CA, Doubal F, Keir S, Sudlow CL, Wardlaw JM, Al-Shahi Salman R. improving interrater agreement about brain microbleeds: development of the Brain Observer MicroBleed Scale (BOMBS). Stroke. 2009; 40:94-99. doi.org/10.1161/STROKEAHA.108.526996
26. Potter GM, Chappell FM, Morris Z, Wardlaw JM. Cerebral perivascular spaces visible on magnetic resonance imaging: development of a qualitative rating scale and its observer reliability. Cerebrovasc Dis. 2015; 39:224-31. doi.org/10.1159/000375153
27. Aribisala BS, Wiseman S, Morris Z, Valdés-Hernández MC, Royle NA, Maniega SM, Gow AJ, Corley J, Bastin ME, Starr J, Deary IJ, Wardlaw JM. Circulating inflammatory markers are associated with magnetic resonance imaging-visible perivascular spaces but not directly with white matter hyperintensities. Stroke. 2014; 45:605-07. doi.org/10.1161/STROKEAHA.113.004059
28. Gregoire SM, Chaudhary UJ, Brown MM, Yousry TA, Kallis C, Jäger HR, Werring DJ. The Microbleed Anatomical Rating Scale (MARS): reliability of a tool to map brain microbleeds. Neurology. 2009; 73:1759-66 doi.org/10.1212/WNL.0b013e3181c34a7d
29. Little RJ, Rubin D. Statistical analysis with missing data. 1987. New York: Wiley.
30. Smith EE, O'Donnell M, Dagenais G, Lear SA, Wielgosz A, Sharma M, Poirier P, Stotts G, Black SE, Strother S, Noseworthy MD, Benavente O, Modi J, et al, and PURE Investigators. Early cerebral small vessel disease and brain volume, cognition, and gait. Ann Neurol. 2015; 77:251-61. doi.org/10.1002/ana.24320
31. Romero JR, Preis SR, Beiser A, DeCarli C, Viswanathan A, Martinez-Ramirez S, Kase CS, Wolf PA, Seshadri S. Risk factors, stroke prevention treatments, and prevalence of cerebral microbleeds in the Framingham Heart Study. Stroke. 2014; 45:1492-94. doi.org/10.1161/STROKEAHA.114.004130
32. Marmot MG, Shipley MJ. Do socioeconomic differences in mortality persist after retirement? 25 year follow up of civil servants from the first Whitehall study. BMJ. 1996; 313:1177-80. doi.org/10.1136/bmj.313.7066.1177
33. Rose G, Hamilton PS, Keen H, Reid DD, McCartney P, Jarrett RJ. Myocardial ischaemia, risk factors and death from coronary heart-disease. Lancet. 1977; 1:105-09. doi.org/10.1016/S0140-6736(77)91701-9
34. Smith GD, Shipley MJ, Rose G. Magnitude and causes of socioeconomic differentials in mortality: further evidence from the Whitehall Study. J Epidemiol Community Health. 1990; 44:265-70. doi.org/10.1136/jech.44.4.265
35. Bosma H, Marmot MG, Hemingway H, Nicholson AC, Brunner E, Stansfeld SA. Low job control and risk of coronary heart disease in Whitehall II (prospective cohort) study. BMJ. 1997; 314:558-65. doi.org/10.1136/bmj.314.7080.558
36. Jokela M, Batty GD, Deary IJ, Silventoinen K, Kivimäki M. Sibling analysis of adolescent intelligence and chronic diseases in older adulthood. Ann Epidemiol. 2011; 21:489-96. doi.org/10.1016/j.annepidem.2011.01.008
37. Braveman P, Egerter S, Williams DR. The social determinants of health: coming of age. Annu Rev Public Health. 2011; 32:381-98. doi.org/10.1146/annurev-publhealth-031210-101218
38. Roseboom T, de Rooij S, Painter R. The Dutch famine and its long-term consequences for adult health. Early Hum Dev. 2006; 82:485-91. doi.org/10.1016/j.earlhumdev.2006.07.001
39. Crimmins EM, Saito Y. Trends in healthy life expectancy in the United States, 1970-1990: gender, racial, and educational differences. Soc Sci Med. 2001; 52:1629-41. doi.org/10.1016/S0277-9536(00)00273-2
40. Mackenbach JP, Bos V, Andersen O, Cardano M, Costa G, Harding S, Reid A, Hemström O, Valkonen T, Kunst AE. Widening socioeconomic inequalities in mortality in six Western European countries. Int J Epidemiol. 2003; 32:830-37. doi.org/10.1093/ije/dyg209
41. Murray AD, McNeil CJ, Salarirad S, Whalley LJ, Staff RT. Early life socioeconomic circumstance and late life brain hyperintensities-a population based cohort study. PLoS One. 2014; 9:e88969. doi.org/10.1371/journal.pone.0088969
42. Satizabal CL, Beiser AS, Chouraki V, Chêne G, Dufouil C, Seshadri S. Incidence of Dementia over Three Decades in the Framingham Heart Study. N Engl J Med. 2016; 374:523-32. doi.org/10.1056/NEJMoa1504327
43. Dufouil C, Alpérovitch A, Tzourio C. Influence of education on the relationship between white matter lesions and cognition. Neurology. 2003; 60:831-36. doi.org/10.1212/01.WNL.0000049456.33231.96
44. Lane EM, Paul RH, Moser DJ, Fletcher TD, Cohen RA. Influence of education on subcortical hyperintensities and global cognitive status in vascular dementia. J Int Neuropsychol Soc. 2011; 17:531-36. doi.org/10.1017/S1355617711000324
45. Farfel JM, Nitrini R, Suemoto CK, Grinberg LT, Ferretti RE, Leite RE, Tampellini E, Lima L, Farias DS, Neves RC, Rodriguez RD, Menezes PR, Fregni F, et al, and Brazilian Aging Brain Study Group. Very low levels of education and cognitive reserve: a clinicopathologic study. Neurology. 2013; 81:650-57. doi.org/10.1212/WNL.0b013e3182a08f1b
46. Deary IJ, Strand S, Smith P, Fernandes C. Intelligence and educational achievement. Intelligence. 2007; 35:13-21. doi.org/10.1016/j.intell.2006.02.001
47. Johnson W, Deary IJ, Iacono WG. Genetic and Environmental Transactions Underlying Educational Attainment. Intelligence. 2009; 37:466-78. doi.org/10.1016/j.intell.2009.05.006
48. Valdés Hernández MC, Booth T, Murray C, Gow AJ, Penke L, Morris Z, Maniega SM, Royle NA, Aribisala BS, Bastin ME, Starr JM, Deary IJ, Wardlaw JM. Brain white matter damage in aging and cognitive ability in youth and older age. Neurobiol Aging. 2013; 34:2740-47. doi.org/10.1016/j.neurobiolaging.2013.05.032
49. Karama S, Bastin ME, Murray C, Royle NA, Penke L, Muñoz Maniega S, Gow AJ, Corley J, Valdés Hernández MC, Lewis JD, Rousseau ME, Lepage C, Fonov V, et al. Childhood cognitive ability accounts for associations between cognitive ability and brain cortical thickness in old age. Mol Psychiatry. 2014; 19:555-59. doi.org/10.1038/mp.2013.64
50. Mathers JC, Strathdee G, Relton CL. Induction of epigenetic alterations by dietary and other environmental factors. Adv Genet. 2010; 71:3-39. doi.org/10.1016/B978-0-12-380864-6.00001-8
51. McGuinness D, McGlynn LM, Johnson PC, MacIntyre A, Batty GD, Burns H, Cavanagh J, Deans KA, Ford I, McConnachie A, McGinty A, McLean JS, Millar K, et al. Socio-economic status is associated with epigenetic differences in the pSoBid cohort. Int J Epidemiol. 2012; 41:151-60. doi.org/10.1093/ije/dyr215
52. Borghol N, Suderman M, McArdle W, Racine A, Hallett M, Pembrey M, Hertzman C, Power C, Szyf M. Associations with early-life socio-economic position in adult DNA methylation. Int J Epidemiol. 2012; 41:62-74 doi.org/10.1093/ije/dyr147
53. Giles-Corti B, Donovan RJ. The relative influence of individual, social and physical environment determinants of physical activity. Soc Sci Med. 2002; doi.org/10.1016/S0277-9536(01)00150-2
54. Prochaska JD, Nolen AB, Kelley H, Sexton K, Linder SH, Sullivan J. Social Determinants of Health in Environmental Justice Communities: Examining Cumulative Risk in Terms of Environmental Exposures and Social Determinants of Health. Hum Ecol Risk Assess. 2014; 20:980-94. doi.org/10.1080/10807039.2013.805957
55. Deary IJ, Weiss A, Batty GD. Intelligence and Personality as Predictors of Illness and Death: How Researchers in Differential Psychology and Chronic Disease Epidemiology Are Collaborating to Understand and Address Health Inequalities. Psychol Sci Public Interest. 2010; 11:53-79. doi.org/10.1177/1529100610387081
56. Barbeau EM, Krieger N, Soobader MJ. Working class matters: socioeconomic disadvantage, race/ethnicity, gender, and smoking in NHIS 2000. Am J Public Health. 2004; 94:269-78. doi.org/10.2105/AJPH.94.2.269
57. Cutler DM, Lleras-Muney A. Education and Health: Evaluating Theories and Evidence. National Bureau of Economic Research Working Paper Series. 2006; No. 12352.
58. Gale CR, Booth T, Starr JM, Deary IJ. Intelligence and socioeconomic position in childhood in relation to frailty and cumulative allostatic load in later life: the Lothian Birth Cohort 1936. J Epidemiol Community Health. 2016; 70:576-82. doi.org/10.1136/jech-2015-205789
59. van Dijk EJ, Prins ND, Vrooman HA, Hofman A, Koudstaal PJ, Breteler MM. Progression of cerebral small vessel disease in relation to risk factors and cognitive consequences: rotterdam Scan study. Stroke. 2008; 39:2712-19. doi.org/10.1161/STROKEAHA.107.513176
60. Benavente O, Pearce LA, Andersen D, Bazan C, Hart RG. MRI Predictors of Stroke Recurrence in Patients with Recent Lacunar Stroke. J Stroke Cerebrovasc Dis. 2014; 4:618-24.
61. Deary I, Whalley LJ, Starr J. A lifetime of intelligence: follow-up studies of the Scottish Mental Surveys of 1932 and 1947: American Psychological Association. 2009.
62. Deary IJ, Pattie A, Starr JM. The stability of intelligence from age 11 to age 90 years: the Lothian birth cohort of 1921. Psychol Sci. 2013; 24:2361-68. doi.org/10.1177/0956797613486487
63. Gow AJ, Johnson W, Pattie A, Brett CE, Roberts B, Starr JM, Deary IJ. Stability and change in intelligence from age 11 to ages 70, 79, and 87: the Lothian Birth Cohorts of 1921 and 1936. Psychol Aging. 2011; 26:232-40. doi.org/10.1037/a0021072
64. Salarirad S, Staff RT, Fox HC, Deary IJ, Whalley L, Murray AD. Childhood intelligence and brain white matter hyperintensities predict fluid intelligence age 78-81 years: a 1921 Aberdeen birth cohort study. Age Ageing. 2011; 40:562-67. doi.org/10.1093/ageing/afr065
65. Benyamin B, Wilson V, Whalley LJ, Visscher PM, Deary IJ. Large, consistent estimates of the heritability of cognitive ability in two entire populations of 11-yearold twins from Scottish mental surveys of 1932 and 1947 Behav Genet. 2005; 35:525-34. doi.org/10.1007/s10519-005-3556-x