Elevated blood pressure is associated with advanced brain aging in mid-life: A 30-year follow-up of The CARDIA Study
Christina S. Dintica
University of California, San Francisco, San Francisco, California, USA
Search for more papers by this authorMohamad Habes
University of Pennsylvania, Philadelphia, Pennsylvania, USA
Neuroimage Analytics Laboratory (NAL) and the Biggs Institute Neuroimaging Core (BINC), Glenn Biggs Institute for Alzheimer's & Neurodegenerative Diseases, University of Texas Health Science Center San Antonio (UTHSCSA), San Antonio, Texas, USA
Search for more papers by this authorGuray Erus
National Institute on Aging, Baltimore, Maryland, USA
Search for more papers by this authorEric Vittinghoff
University of California, San Francisco, San Francisco, California, USA
Search for more papers by this authorChristos Davatzikos
University of Pennsylvania, Philadelphia, Pennsylvania, USA
Search for more papers by this authorIlya M. Nasrallah
University of Pennsylvania, Philadelphia, Pennsylvania, USA
Search for more papers by this authorLenore J. Launer
National Institute on Aging, Baltimore, Maryland, USA
Search for more papers by this authorStephen Sidney
Kaiser Permanente Northern California, Oakland, California, USA
Search for more papers by this authorCorresponding Author
Kristine Yaffe
University of California, San Francisco, San Francisco, California, USA
Correspondence
Kristine Yaffe, Department of Psychiatry, University of California, San Francisco, 4150 Clement Street, San Francisco, CA 94121, USA.
E-mail: [email protected]
Search for more papers by this authorChristina S. Dintica
University of California, San Francisco, San Francisco, California, USA
Search for more papers by this authorMohamad Habes
University of Pennsylvania, Philadelphia, Pennsylvania, USA
Neuroimage Analytics Laboratory (NAL) and the Biggs Institute Neuroimaging Core (BINC), Glenn Biggs Institute for Alzheimer's & Neurodegenerative Diseases, University of Texas Health Science Center San Antonio (UTHSCSA), San Antonio, Texas, USA
Search for more papers by this authorGuray Erus
National Institute on Aging, Baltimore, Maryland, USA
Search for more papers by this authorEric Vittinghoff
University of California, San Francisco, San Francisco, California, USA
Search for more papers by this authorChristos Davatzikos
University of Pennsylvania, Philadelphia, Pennsylvania, USA
Search for more papers by this authorIlya M. Nasrallah
University of Pennsylvania, Philadelphia, Pennsylvania, USA
Search for more papers by this authorLenore J. Launer
National Institute on Aging, Baltimore, Maryland, USA
Search for more papers by this authorStephen Sidney
Kaiser Permanente Northern California, Oakland, California, USA
Search for more papers by this authorCorresponding Author
Kristine Yaffe
University of California, San Francisco, San Francisco, California, USA
Correspondence
Kristine Yaffe, Department of Psychiatry, University of California, San Francisco, 4150 Clement Street, San Francisco, CA 94121, USA.
E-mail: [email protected]
Search for more papers by this authorAbstract
Background
High blood pressure (BP) is a risk factor for late-life brain health; however, the association of elevated BP with brain health in mid-life is unclear.
Methods
We identified 661 participants from the Coronary Artery Risk Development in Young Adults Study (age 18–30 at baseline) with 30 years of follow-up and brain magnetic resonance imaging at year 30. Cumulative exposure of BP was estimated by time-weighted averages (TWA). Ideal cardiovascular health was defined as systolic BP < 120 mm Hg, diastolic BP < 80 mm Hg. Brain age was calculated using previously validated high dimensional machine learning pattern analyses.
Results
Every 5 mmHg increment in TWA systolic BP was associated with approximately 1-year greater brain age (95% confidence interval [CI]: 0.50–1.36) Participants with TWA systolic or diastolic BP over the recommended guidelines for ideal cardiovascular health, had on average 3-year greater brain age (95% CI: 1.00–4.67; 95% CI: 1.45–5.13, respectively).
Conclusion
Elevated BP from early to mid adulthood, even below clinical cut-offs, is associated with advanced brain aging in mid-life.
CONFLICTS OF INTEREST
The authors declare that there are no conflicts of interest.
Supporting Information
Filename | Description |
---|---|
alz12725-sup-0001-SuppMat.pdf1.1 MB | Supporting Information |
alz12725-sup-0002-TableS1.docx13.3 KB | Supporting Information |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Qiu C. Preventing Alzheimer's disease by targeting vascular risk factors: hope and gap. J Alzheimer's Dis 2012; 32: 721-31. https://doi.org/10.3233/JAD-2012-120922
- 2Barnes DE, Yaffe K. The projected effect of risk factor reduction on Alzheimer's disease prevalence. Lancet Neurol 2011; 10: 819-28. https://doi.org/10.1016/S1474-4422(11)70072-2
- 3Iadecola C, Yaffe K, Biller J, et al. Impact of hypertension on cognitive function: a scientific statement from the American Heart Association. Hypertension 2016; 68. https://doi.org/10.1161/HYP.0000000000000053
- 4Habes M, Erus G, Toledo JB, et al. White matter hyperintensities and imaging patterns of brain ageing in the general population. Brain 2016; 139: 1164-79. https://doi.org/10.1093/brain/aww008
- 5Williamson JD, Pajewski NM, Auchus AP, et al. Effect of intensive vs standard blood pressure control on probable dementia. JAMA 2019; 321: 553. https://doi.org/10.1001/jama.2018.21442
- 6Yaffe K, Vittinghoff E, Pletcher MJ, et al. Early adult to midlife cardiovascular risk factors and cognitive function. Circulation 2014; 129: 1560-7. https://doi.org/10.1161/CIRCULATIONAHA.113.004798
- 7Mahinrad S, Kurian S, Garner CR, et al. Cumulative blood pressure exposure during young adulthood and mobility and cognitive function in midlife. Circulation 2020; 141: 712-24. https://doi.org/10.1161/CIRCULATIONAHA.119.042502
- 8Fjell AM, McEvoy L, Holland D, Dale AM, Walhovd KB. What is normal in normal aging? Effects of aging, amyloid and Alzheimer's disease on the cerebral cortex and the hippocampus. Prog Neurobiol 2014; 117: 20-40. https://doi.org/10.1016/j.pneurobio.2014.02.004
- 9Habes M, Janowitz D, Erus G, et al. Advanced brain aging: relationship with epidemiologic and genetic risk factors, and overlap with Alzheimer's disease atrophy patterns. Transl Psychiatry 2016; 6: e775–e775. https://doi.org/10.1038/tp.2016.39
- 10Habes M, Pomponio R, Shou H, et al. The Brain Chart of Aging: Machine-learning analytics reveals links between brain aging, White matter disease, amyloid burden, and cognition in the iSTAGING consortium of 10,216 harmonized MR scans. Alzheimer's Dement 2021; 17: 89-102. https://doi.org/10.1002/alz.12178
- 11Cole JH, Franke K. Predicting age using neuroimaging: innovative brain ageing biomarkers. Trends Neurosci 2017; 40: 681-90. https://doi.org/10.1016/j.tins.2017.10.001
- 12Friedman GD, Cutter GR, Donahue RP, et al. Cardia: study design, recruitment, and some characteristics of the examined subjects. J Clin Epidemiol 1988; 41: 1105-16. https://doi.org/10.1016/0895-4356(88)90080-7
- 13Launer LJ, Lewis CE, Schreiner PJ, et al. Vascular factors and multiple measures of early brain health: CARDIA Brain MRI Study. PLoS One 2015; 10:e0122138. https://doi.org/10.1371/journal.pone.0122138
- 14Lloyd-Jones DM, Hong Y, Labarthe D, et al. Defining and setting national goals for cardiovascular health promotion and disease reduction: the American Heart Association's strategic Impact Goal through 2020 and beyond. Circulation 2010; 121: 586-613. https://doi.org/10.1161/CIRCULATIONAHA.109.192703
- 15Goldszal AF, Davatzikos C, Pham DL, Yan MXH, Bryan RN, Resnick SM. An image-processing system for qualitative and quantitative volumetric analysis of brain images. J Comput Assist Tomogr 1998; 22: 827-37. https://doi.org/10.1097/00004728-199809000-00030
- 16Dinggang Shen, Davatzikos C. HAMMER: hierarchical attribute matching mechanism for elastic registration. IEEE Trans Med Imaging 2002; 21: 1421-39. https://doi.org/10.1109/TMI.2002.803111
- 17Zacharaki EI, Kanterakis S, Bryan RN, Davatzikos C. Measuring Brain Lesion Progression with a Supervised Tissue Classification System, 2008, p. 620-7. https://doi.org/10.1007/978-3-540-85988-8_74
- 18Tustison NJ, Avants BB, Cook PA, et al. N4ITK: Improved N3 Bias Correction. IEEE Trans Med Imaging 2010; 29: 1310-20. https://doi.org/10.1109/TMI.2010.2046908
- 19Doshi J, Erus G, Ou Y, Gaonkar B, Davatzikos C. Multi-Atlas Skull-Stripping. Acad Radiol 2013; 20: 1566-76. https://doi.org/10.1016/j.acra.2013.09.010
- 20Doshi J, Erus G, Ou Y, et al. MUSE: MUlti-atlas region Segmentation utilizing Ensembles of registration algorithms and parameters, and locally optimal atlas selection. Neuroimage 2016; 127: 186-95. https://doi.org/10.1016/j.neuroimage.2015.11.073
- 21Eavani H, Habes M, Satterthwaite TD, et al. Heterogeneity of structural and functional imaging patterns of advanced brain aging revealed via machine learning methods. Neurobiol Aging 2018; 71: 41-50. https://doi.org/10.1016/j.neurobiolaging.2018.06.013
- 22Habes M, Erus G, Toledo JB, et al. Regional tract-specific White matter hyperintensities are associated with patterns of aging-related brain atrophy via vascular risk factors, but also independently. Alzheimer's Dement Diagnosis, Assess Dis Monit 2018; 10: 278-84. https://doi.org/10.1016/j.dadm.2018.02.002
- 23Le TT, Kuplicki RT, McKinney BA, Yeh H-W, Thompson WK, Paulus MP. A nonlinear simulation framework supports adjusting for age when analyzing BrainAGE. Front Aging Neurosci 2018; 10. https://doi.org/10.3389/fnagi.2018.00317
- 24Reis JP, Loria CM, Launer LJ, et al. Cardiovascular health through young adulthood and cognitive functioning in midlife. Ann Neurol 2013; 73: 170-9. https://doi.org/10.1002/ana.23836
- 25Kamboh MI, Ferrell RE, Kottke B. Genetic studies of human apolipoproteins. V. A novel rapid procedure to screen apolipoprotein E polymorphism. J Lipid Res 1988; 29: 1535-43.
- 26Xiong C, Luo J, Coble D, Agboola F, Kukull W, Morris JC. Complex interactions underlie racial disparity in the risk of developing Alzheimer's disease dementia. Alzheimer's Dement 2020; 16: 589–97. https://doi.org/10.1002/alz.12060
- 27Levine DA, Gross AL, Briceño EM, et al. Association Between Blood Pressure and Later-Life Cognition Among Black and White Individuals. JAMA Neurol 2020; 77: 810. https://doi.org/10.1001/jamaneurol.2020.0568
- 28Caunca MR, Odden MC, Glymour MM, et al. Association of racial residential segregation throughout young adulthood and cognitive performance in middle-aged participants in the CARDIA Study. JAMA Neurol 2020; 77: 1000. https://doi.org/10.1001/jamaneurol.2020.0860
- 29Korf ESC, White LR, Scheltens P, Launer LJ. Midlife blood pressure and the risk of hippocampal atrophy. Hypertension 2004; 44: 29-34. https://doi.org/10.1161/01.HYP.0000132475.32317.bb
- 30Beauchet O, Celle S, Roche F, et al. Blood pressure levels and brain volume reduction. J Hypertens 2013; 31: 1502-16. https://doi.org/10.1097/HJH.0b013e32836184b5
- 31Suvila K, Lima JAC, Yano Y, Tan ZS, Cheng S, Niiranen TJ. Early-but not late-onset hypertension is related to midlife cognitive function. Hypertension 2021: 972-9. https://doi.org/10.1161/HYPERTENSIONAHA.120.16556
- 32Lane CA, Barnes J, Nicholas JM, et al. Associations between blood pressure across adulthood and late-life brain structure and pathology in the neuroscience substudy of the 1946 British birth cohort (Insight 46): an epidemiological study. Lancet Neurol 2019; 18: 942-52. https://doi.org/10.1016/S1474-4422(19)30228-5
- 33Pantoni L, Simoni M. Pathophysiology of cerebral small vessels in vascular cognitive impairment. Int Psychogeriatrics 2003; 15: 59-65. https://doi.org/10.1017/S1041610203008974
- 34Wartolowska KA, Webb AJS. Midlife blood pressure is associated with the severity of white matter hyperintensities: analysis of the UK Biobank cohort study. Eur Heart J 2021; 42: 750-7. https://doi.org/10.1093/eurheartj/ehaa756
- 35Lane CA, Barnes J, Nicholas JM, et al. Associations between blood pressure across adulthood and late-life brain structure and pathology in the neuroscience substudy of the 1946 British birth cohort (Insight 46): an epidemiological study. Lancet Neurol 2019; 18: 942-52. https://doi.org/10.1016/S1474-4422(19)30228-5
- 36Yaffe K, Bahorik AL, Hoang TD, et al. Cardiovascular risk factors and accelerated cognitive decline in midlife. Neurology 2020; 95: e839-46. https://doi.org/10.1212/WNL.0000000000010078
- 37Sun D, Thomas EA, Launer LJ, Sidney S, Yaffe K, Fornage M. Association of blood pressure with cognitive function at midlife: A Mendelian randomization study. BMC Med Genomics 2020; 13: 1-9. https://doi.org/10.1186/s12920-020-00769-y
- 38Smith EE, Beaudin AE. New insights into cerebral small vessel disease and vascular cognitive impairment from MRI. Curr Opin Neurol 2018; 31: 36-43. https://doi.org/10.1097/WCO.0000000000000513
- 39Maillard P, Seshadri S, Beiser A, et al. Effects of systolic blood pressure on White-matter integrity in young adults in the Framingham Heart Study: a cross-sectional study. Lancet Neurol 2012; 11: 1039-47. https://doi.org/10.1016/S1474-4422(12)70241-7
- 40McNeil CJ, Myint PK, Sandu A-L, et al. Increased diastolic blood pressure is associated with MRI biomarkers of dementia-related brain pathology in normative ageing. Age Ageing 2018; 47: 95-100. https://doi.org/10.1093/ageing/afx102