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The prospective relationship between prehypertension, race, and whole-brain white matter microstructure

Abstract

Compared with whites, blacks develop hypertension earlier in life, progress from prehypertension to hypertension at an accelerated rate, and exhibit greater hypertension-mediated organ damage (e.g., kidney disease, stroke). In this paper, we tested whether the longitudinal associations between elevated systolic blood pressure and disruption of brain white matter structural integrity differ as a function of race. A community sample of 100 middle-aged adults with prehypertension underwent diffusion imaging to quantify indirect metrics of white matter structural integrity, including fractional anisotropy. Blood pressure and diffusion imaging measurements were collected at baseline and at a 2-year follow-up. Regression analyses showed that higher systolic blood pressure at baseline was associated with a decrease in fractional anisotropy over 2 years in blacks only (β = −0.51 [95% CI = −0.85, −0.16], t = −2.93, p = 0.004, ΔR2 = 0.09). These findings suggest that blacks are more susceptible to the impact of systolic prehypertension on white matter structural integrity.

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References

  1. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, et al. Heart disease and stroke statistics—2012 update: a report from the American Heart Association. Circulation. 2012;125:e2–e220.

    Article  Google Scholar 

  2. Williams B, Mancia G, Spiering W, Agabiti Rosei E, Azizi M, Burnier M, et al. 2018 ESC/ESH Guidelines for the management of arterial hypertension. Eur Heart J. 2018;39:3021–104.

    Article  Google Scholar 

  3. Faraco G, Iadecola C. Hypertension: a harbinger of stroke and dementia. Hypertension. 2013;62:810–7.

    Article  CAS  Google Scholar 

  4. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9:689–701.

    Article  Google Scholar 

  5. Scuteri A, Wang H. Pulse wave velocity as a marker of cognitive impairment in the elderly. J Alzheimers Dis. 2014;42(s4):S401–S10.

    Article  Google Scholar 

  6. Pantoni L, Garcia JH, Gutierrez JA. Cerebral white matter is highly vulnerable to ischemia. Stroke. 1996;27:1641–7.

    Article  CAS  Google Scholar 

  7. Aribisala BS, Morris Z, Eadie E, Thomas A, Gow A, Hernández MCV, et al. Blood pressure, internal carotid artery flow parameters, and age-related white matter hyperintensities. Hypertension. 2014;113:02735. HYPERTENSIONAHA

    Google Scholar 

  8. Launer LJ, Lewis CE, Schreiner PJ, Sidney S, Battapady H, Jacobs DR, et al. Vascular factors and multiple measures of early brain health: CARDIA brain MRI study. PLoS ONE. 2015;10:e0122138.

    Article  Google Scholar 

  9. Haight T, Bryan RN, Erus G, Hsieh M-K, Davatzikos C, Nasrallah I, et al. White matter microstructure, white matter lesions, and hypertension: an examination of early surrogate markers of vascular-related brain change in midlife. NeuroImage: Clin. 2018;18:753–61.

    Article  Google Scholar 

  10. Allen B, Muldoon MF, Gianaros PJ, Jennings JR. Higher blood pressure partially links greater adiposity to reduced brain white matter integrity. Am J Hypertens. 2016;29:1029–37.

    Article  Google Scholar 

  11. Maillard P, Seshadri S, Beiser A, Himali JJ, Au R, Fletcher E, 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.

    Article  Google Scholar 

  12. Song S-K, Sun S-W, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage. 2002;17:1429–36.

    Article  Google Scholar 

  13. Song S-K, Sun S-W, Ju W-K, Lin S-J, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage. 2003;20:1714–22.

    Article  Google Scholar 

  14. Horsfield MA, Jones DK. Applications of diffusion‐weighted and diffusion tensor MRI to white matter diseases–a review. NMR Biomed. 2002;15:570–7.

    Article  Google Scholar 

  15. Yusuf S, Reddy S, Ôunpuu S, Anand S. Global burden of cardiovascular diseases: part I: general considerations, the epidemiologic transition, risk factors, and impact of urbanization. Circulation. 2001;104:2746–53.

    Article  CAS  Google Scholar 

  16. Selassie A, Wagner CS, Laken ML, Ferguson ML, Ferdinand KC, Egan BM. Progression is accelerated from prehypertension to hypertension in blacks. Hypertension. 2011;58:579–87.

    Article  CAS  Google Scholar 

  17. Chaturvedi N, Bulpitt CJ, Leggetter S, Schiff R, Nihoyannopoulos P, Strain WD, et al. Ethnic differences in vascular stiffness and relations to hypertensive target organ damage. J Hypertens. 2004;22:1731–7.

    Article  CAS  Google Scholar 

  18. Brickman AM, Schupf N, Manly JJ, Luchsinger JA, Andrews H, Tang MX, et al. Brain morphology in older African Americans, Caribbean Hispanics, and whites from northern Manhattan. Arch Neurol. 2008;65:1053–61.

    PubMed  PubMed Central  Google Scholar 

  19. Forouzanfar MH, Afshin A, Alexander LT, Anderson HR, Bhutta ZA, Biryukov S, et al. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388:1659–724.

    Article  Google Scholar 

  20. Gianaros PJ, Marsland AL, Sheu LK, Erickson KI, Verstynen TD. Inflammatory pathways link socioeconomic inequalities to white matter architecture. Cereb Cortex. 2012;23:2058–71.

    Article  Google Scholar 

  21. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL,Jr et al. The seventh report of the joint national committee on prevention, detection, evaluation, and treatment of high blood pressure: the JNC 7 report. JAMA. 2003;289:2560–71.

    Article  CAS  Google Scholar 

  22. Pickering TG, Hall JE, Appel LJ, Falkner BE, Graves J, Hill MN, et al. Recommendations for blood pressure measurement in humans and experimental animals: part 1: blood pressure measurement in humans: a statement for professionals from the Subcommittee of Professional and Public Education of the American Heart Association Council on High Blood Pressure Research. Circulation. 2005;111:697–716.

    Article  Google Scholar 

  23. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17:143–55.

    Article  Google Scholar 

  24. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage. 2006;31:1487–505.

    Article  Google Scholar 

  25. Hayes AF. Introduction to mediation, moderation, and conditional process analysis: a regression-based approach: Guilford Publications; New York, NY, 2017.

  26. Aickin M. Dealing with change: using the conditional change model for clinical research. Prem J. 2009;13:80.

    Google Scholar 

  27. Johnson PO, Neyman J. Tests of certain linear hypotheses and their application to some educational problems. Statistical research memoirs. 1936;1:57–93.

  28. Preacher KJ, Curran PJ, Bauer DJ. Computational tools for probing interactions in multiple linear regression, multilevel modeling, and latent curve analysis. J Educ Behav Stat. 2006;31:437–48.

    Article  Google Scholar 

  29. Seo Y, Kim G-T, Choi JW. Early detection of neonatal hypoxic–ischemic white matter injury: an MR diffusion tensor imaging study. Neuroreport. 2017;28:845.

    Article  CAS  Google Scholar 

  30. Wang S, Wu EX, Tam CN, Lau H-F, Cheung P-T, Khong P-L. Characterization of white matter injury in a hypoxic-ischemic neonatal rat model by diffusion tensor MRI. Stroke. 2008;39:2348–53.

    Article  Google Scholar 

  31. Iadecola C. The pathobiology of vascular dementia. Neuron. 2013;80:844–66.

    Article  CAS  Google Scholar 

  32. Rosenberg GA. Inflammation and white matter damage in vascular cognitive impairment. Stroke. 2009;40(3 suppl 1):S20–S3.

    Article  Google Scholar 

  33. Power MC, Tingle JV, Reid RI, Huang J, Sharrett AR, Coresh J, et al. Midlife and late‐life vascular risk factors and white matter microstructural integrity: the atherosclerosis risk in communities neurocognitive study. J Am Heart Assoc. 2017;6:e005608.

    Article  Google Scholar 

  34. Rosano C, Abebe KZ, Aizenstein HJ, Boudreau R, Jennings JR, Venkatraman V, et al. Longitudinal systolic blood pressure characteristics and integrity of white matter tracts in a cohort of very old black and white adults. Am J Hypertens. 2014;28:326–34.

    Article  Google Scholar 

  35. Suzuki H, Gao H, Bai W, Evangelou E, Glocker B, O’Regan DP, et al. Abnormal brain white matter microstructure is associated with both pre-hypertension and hypertension. PLoS ONE. 2017;12:e0187600.

    Article  Google Scholar 

  36. Morgello S, Murray J, Van Der Elst S, Byrd D. HCV, but not HIV, is a risk factor for cerebral small vessel disease. Neurol-Neuroimmunol Neuroinflamm. 2014;1:e27.

    Article  Google Scholar 

  37. Rostand SG, Cross SK, Kirk KA, Lee JY, Kuhlmann A, Amann K. Racial differences in renal arteriolar structure in children with minimal change nephropathy. Kidney Int. 2005;68:1154–60.

    Article  Google Scholar 

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Acknowledgements

This study was supported by grants from the (National Heart Lung and Blood Institute (HL101959, HL089850, and HL007560)).

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Correspondence to Ben Allen.

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Allen, B., Muldoon, M.F., Gianaros, P.J. et al. The prospective relationship between prehypertension, race, and whole-brain white matter microstructure. J Hum Hypertens 34, 82–89 (2020). https://doi.org/10.1038/s41371-019-0184-0

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