Prehypertensive blood pressures and regional cerebral blood flow independently relate to cognitive performance in midlife

Journal of the American Heart Association

Volumn 6, Issue 3, 2017, Pages

  Jennings, J Richard ^a   Muldoon, Matthew F ^a   Ryan, Christopher ^a,b   Gach, H Michael ^a,c   Heim, Alicia ^a   Sheu, Lei K ^a   Gianaros, Peter J ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WASHINGTON UNIVERSITY   (United States)

Author keywords

Cognition; Magnetic resonance imaging; Middle age; Prehypertension; Regional blood flow

Indexed keywords

ADULT; ARTERIAL SPIN LABELING; ARTICLE; BRAIN BLOOD FLOW; BRAIN REGION; COGNITION; CONTROLLED STUDY; EXECUTIVE FUNCTION; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; MEMORY; MENTAL TASK; MIDDLE AGED; NEUROIMAGING; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PREHYPERTENSION; PRIORITY JOURNAL; SYSTOLIC BLOOD PRESSURE; WORKING MEMORY; BLOOD PRESSURE; BRAIN CIRCULATION; DIAGNOSTIC IMAGING; FUNCTIONAL NEUROIMAGING; NORMAL HUMAN; PATHOPHYSIOLOGY; PHYSIOLOGY; SHORT TERM MEMORY; TASK PERFORMANCE; VASCULARIZATION;

SPIN LABEL;

ADULT; BLOOD PRESSURE; CEREBROVASCULAR CIRCULATION; CEREBRUM; COGNITION; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL NEUROIMAGING; HEALTHY VOLUNTEERS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; MEMORY, SHORT-TERM; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PREHYPERTENSION; SPIN LABELS; TASK PERFORMANCE AND ANALYSIS;

EID: 85032579519     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.116.004856     Document Type: Article

References (75)

1. 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, Arnett DK, Bennett DA, Chui HC, Higashida RT, Lindquist R, Nilsson PM, Roman GC, Sellke FW, Seshadri S. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2011;42:2672-2713.
2. Hughes TM, Sink KM. Hypertension and its role in cognitive function: current evidence and challenges for the future. Am J Hypertens. 2016;29:149-157.
3. Tzourio C, Laurent S, Debette S. Is hypertension associated with an accelerated aging of the brain? Hypertension. 2014;63:894-903.
4. Launer LJ, Lewis CE, Schreiner PJ, Sidney S, Battapady H, Jacobs DR, Lim KO, D'Esposito M, Zhang Q, Reis J, Davatzikos C, Bryan RN. Vascular factors and multiple measures of early brain health: CARDIA brain MRI study. PLoS One. 2015;10:e0122138.
5. Elias MF, Goodell AL, Dore GA. Hypertension and cognitive functioning: a perspective in historical context. Hypertension. 2012;60:260-268.
6. Iadecola C, Yaffe K, Biller J, Bratzke LC, Faraci FM, Gorelick PB, Gulati M, Kamel H, Knopman DS, Launer LJ, Saczynski JS, Seshadri S, Zeki A-HA. Impact of hypertension on cognitive function: a scientific statement from the American Heart Association. Hypertension. 2016;68:e67-e94.
7. Esler M, Eikelis N, Schlaich M, Lambert G, Alvarenga M, Dawood T, Kaye D, Barton D, Pier C, Guo L, Brenchley C, Jennings G, Lambert E. Chronic mental stress is a cause of essential hypertension: presence of biological markers of stress. Clin Exp Pharmacol Physiol. 2008;35:498-502.
8. Sved AF, Ito S, Sved JC. Brainstem mechanisms of hypertension: role of the rostral ventrolateral medulla. Curr Hypertens Rep. 2003;5:262-268.
9. Benarroch EE. The central autonomic network: functional organization, dysfunction, and perspective. Mayo Clin Proc. 1993;68:988-1001.
10. Shoemaker JK, Goswami R. Forebrain neurocircuitry associated with human reflex cardiovascular control. Front Physiol. 2015;6:1-14.
11. Gianaros PJ, Sheu LK. A review of neuroimaging studies of stressor-evoked blood pressure reactivity: emerging evidence for a brain-body pathway to coronary heart disease risk. Neuroimage. 2009;47:922-936.
12. Jennings JR, Muldoon MF, Ryan C, Price JC, Greer P, Sutton-Tyrrell K, van der Veen FM, Meltzer CC. Reduced cerebral blood flow response and compensation among patients with untreated hypertension. Neurology. 2005;64:1358-1365.
13. Jennings JR, Mendelson DN, Muldoon MF, Ryan CM, Gianaros PJ, Raz N, Aizenstein H. Regional grey matter shrinks in hypertensive individuals despite successful lowering of blood pressure. J Hum Hypertens. 2012;26:295-305.
14. Jennings JR, Muldoon MF, Price J, Christie IC, Meltzer CC. Cerebrovascular support for cognitive processing in hypertensive patients is altered by blood pressure treatment. Hypertension. 2008;52:65-71.
15. Jennings JR, Zanstra Y. Is the brain the essential in hypertension? Neuroimage. 2009;47:914-921.
16. Waldstein SR, Giggey PP, Thayer JF, Zonderman AB. Nonlinear relations of blood pressure to cognitive function: the Baltimore Longitudinal Study of Aging. Hypertension. 2005;45:374-379.
17. Waldstein SR, Jennings JR, Ryan CM, Muldoon MF, Shapiro AP, Pleferone JM, Fazzari TV, Manuck SB. Hypertension and neuropsychological performance in men: interactive effects of age. Health Psychol. 1996;15:102-109.
18. Jennings JR, Muldoon MF, Ryan CM, Mintun MA, Meltzer CC, Townsend DW, Sutton-Tyrrell K, Shapiro AP, Manuck SB. Cerebral blood flow in hypertensive patients: an initial report of reduced and compensatory blood flow responses during performance of two cognitive tasks. Hypertension. 1998;31:1216-1222.
19. Dai W, Lopez OL, Carmichael OT, Becker JT, Kuller LH, Gach HM. Abnormal regional cerebral blood flow in cognitively normal elderly subjects with hypertension. Stroke. 2008;39:349-354.
20. Haight TJ, Bryan RN, Erus G, Davatzikos C, Jacobs DR, D'Esposito M, Lewis CE, Launer LJ. Vascular risk factors, cerebrovascular reactivity, and the defaultmode brain network. Neuroimage. 2015;115:7-16.
21. Steffener J, Brickman AM, Habeck CG, Salthouse TA, Stern Y. Cerebral blood flow and gray matter volume covariance patterns of cognition in aging. Hum Brain Mapp. 2013;34:3267-3279.
22. Nelson HE, Willison JR, Nelson HE. National Adult Reading Test (NART) Test Manual. Windsor: NFER-Nelson; 1991.
23. Bastianello S, Bozzao A, Paolillo A, Giugni E, Gasperini C, Koudriavtseva T, Millefiorini E, Horsfield MA, Colonnese C, Toni D, Fiorelli M, Pozzilli C, Bozzao L. Fast fluid-attenuated inversion-recovery versus conventional spin-echo sequences for MR quantification of multiple sclerosis lesions. AJNR Am J Neuroradiol. 1997;18:699-704.
24. Dai W, Garcia D, de Bazelaire C, Alsop DC. Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn Reson Med. 2008;60:1488-1497.
25. Wang J, Aguirre GK, Kimberg DY, Roc AC, Li L, Detre JA. Arterial spin labeling perfusion fMRI with very low task frequency. Magn Reson Med. 2003;49:796-802.
26. Buxton RB, Frank LR, Wong EC, Siewert B, Warach S, Edelman RR. A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med. 1998;40:383-396.
27. Bush G, Shin LM. The Multi-Source Interference Task: an fMRI task that reliably activates the cingulo-frontal-parietal cognitive/attention network. Nat Protoc. 2006;1:308-313.
28. Sheu LK, Jennings JR, Gianaros PJ. Test-retest reliability of an fMRI paradigm for studies of cardiovascular reactivity. Psychophysiology. 2012;49:873-884.
29. Wang Z, Aguirre GK, Rao H, Wang J, Fernandez-Seara MA, Childress AR, Detre JA. Empirical optimization of ASL data analysis using an ASL data processing toolbox: ASLtbx. Magn Reson Imaging. 2008;26:261-269.
30. Beason-Held LL, Thambisetty M, Deib G, Sojkova J, Landman BA, Zonderman AB, Ferrucci L, Kraut MA, Resnick SM. Baseline cardiovascular risk predicts subsequent changes in resting brain function. Stroke. 2012;43:1542-1547.
31. Beissner F, Meissner K, Bar KJ, Napadow V. The autonomic brain: an activation likelihood estimation meta-analysis for central processing of autonomic function. J Neurosci. 2013;33:10503-10511.
32. Verberne AJ, Owens NC. Cortical modulation of the cardiovascular system. Prog Neurobiol. 1998;54:149-168.
33. Gianaros PJ, Derbyshire SW, May JC, Siegle GJ, Gamalo MA, Jennings JR. Anterior cingulate activity correlates with blood pressure during stress. Psychophysiology. 2005;42:627-635.
34. Gianaros PJ, Greer PJ, Ryan CM, Jennings JR. Higher blood pressure predicts lower regional grey matter volume: consequences on short-term information processing. Neuroimage. 2006;31:754-765.
35. Gianaros PJ, Jennings JR, Sheu LK, Derbyshire SW, Matthews KA. Heightened functional neural activation to psychological stress covaries with exaggerated blood pressure reactivity. Hypertension. 2007;49:134-140.
36. Gianaros PJ, Sheu LK, Matthews KA, Jennings JR, Manuck SB, Hariri AR. Individual differences in stressor-evoked blood pressure reactivity vary with activation, volume, and functional connectivity of the amygdala. J Neurosci. 2008;28:990-999.
37. Gianaros PJ, Wager TD. Brain-body pathways linking psychological stress and physical health. Curr Dir Psychol Sci. 2015;24:313-321.
38. Baer K-J, de la Cruz F, Schumann A, Bar KJ, Koehler S, Sauer H, Critchley H, Wagner G. Functional connectivity and network analysis of midbrain and brainstem nuclei. Neuroimage. 2016;134:53-63.
39. Dum RP, Levinthal DJ, Strick PL. Motor, cognitive and affective areas of the cerebral cortex influence the adrenal medulla. Proc Natl Acad Sci USA. 2016;113:9922-9927.
40. Card JP, Sved AF. Central autonomic pathways. In: Llewellyn-Smith IJ, Verberne AJ, eds. Central Regulations of Autonomic Functions. New York: Oxford University Press; 2011:3-22.
41. Dampney RA. The hypothalamus and autonomic regulation: an overview. In: Llewellyn-Smith IJ, Verberne AJ, eds. Central Regulations of Autonomic Functions. New York: Oxford University Press; 2011:47-61.
42. Verberne AJM. Modulation of autonoimc function by the cerebral cortex. In: Llewellyn-Smith IJ, Verberne AJ, eds. Central Regulations of Autonomic Functions. New York: Oxford University Press; 2011:202-219.
43. Longstreth WT Jr, Manolio TA, Arnold A, Burke GL, Bryan N, Jungreis CA, Enright P, O'Leary D, Fried L. Clinical correlates of white matter findings on cranial magnetic resonance imaging of 3301 elderly people. The Cardiovascular Health Study. Stroke. 1996;27:1274-1282.
44. Cohen S, Kamarck T, Mermelstein R. A global measure of perceived stress. J Health Soc Behav. 1983;24:385-396.
45. Winters-Hart C, Brach SK, Trauth KA. Validity of a questionnaire to assess historical physical activity in older women. Med Sci Sports Exerc. 2004;36:2082-2087.
46. Redline S, Strohl KP. Recognition and consequences of obstructive sleep apnea hypopnea syndrome. Clin Chest Med. 1998;19:1-19.
47. Jennings JR, van der Veen FM, Meltzer CC. Verbal and spatial working memory in older individuals: a positron emission tomography study. Brain Res. 2006;1092:177-189.
48. Kohler S, Baars MA, Spauwen P, Schievink S, Verhey FR, van Boxtel MJ. Temporal evolution of cognitive changes in incident hypertension: prospective cohort study across the adult age span. Hypertension. 2014;63:245-251.
49. Swan GE, Carmelli D, Larue A. Systolic blood pressure tracking over 25 to 30 years and cognitive performance in older adults. Stroke. 1998;29:2334-2340.
50. Chen KH, Henderson VW, Stolwyk RJ, Dennerstein L, Szoeke C. Prehypertension in midlife is associated with worse cognition a decade later in middleaged and older women. Age Ageing. 2015;44:439-445.
51. King H, Miller RE. Hypertension: cognitive and behavioral considerations. Neuropsychol Rev. 1990;1:31-73.
52. Waldstein SR, Manuck SB, Ryan CM, Muldoon MF. Neuropsychological correlates of hypertension: review and methodologic considerations. Psychol Bull. 1991;110:451-468.
53. Novak V, Hajjar I. The relationship between blood pressure and cognitive function. Nat Rev Cardiol. 2010;7:686-698.
54. Winklewski PJ, Radkowski M, Demkow U. Relevance of immune-sympathetic nervous system interplay for the development of hypertension. Adv Exp Med Biol. 2016;884:37-43.
55. Jennings JR, Muldoon MF, Whyte EM, Scanlon J, Price J, Meltzer CC. Brain imaging findings predict blood pressure response to pharmacological treatment. Hypertension. 2008;52:1113-1119.
56. Harrison DG. The mosaic theory revisited: common molecular mechanisms coordinating diverse organ and cellular events in hypertension. J Am Soc Hypertens. 2013;7:68-74.
57. Page IH. The mosaic theory of arterial hypertension-its interpretation. Perspect Biol Med. 1967;10:325-333.
58. Johnson RJ, Feig DI, Nakagawa T, Sanchez-Lozada LG, Rodriguez-Iturbe B. Pathogenesis of essential hypertension: historical paradigms and modern insights. J Hypertens. 2008;26:381-391.
59. Black HR, Elliott WJ. Hypertension: A Companion to Braunwald's Heart Disease. Philadelphia, PA: Elsevier Saunders; 2013.
60. Izzo JL Jr, Sica DA, Black HR. Hypertension Primer: [The Essentials of High Blood Pressure: Basic Science, Population Science, and Clinical Management]. 4th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2008.
61. Nishtala A, Himali JJ, Beiser A, Murabito JM, Seshadri S, Wolf PA, Au R. Midlife hypertension risk and cognition in the non-demented oldest old: Framingham Heart Study. J Alzheimers Dis. 2015;47:197-204.
62. Guyenet PG. The sympathetic control of blood pressure. Nat Rev Neurosci. 2006;7:335-346.
63. Gabor A, Leenen FH. Central neuromodulatory pathways regulating sympathetic activity in hypertension. J Appl Physiol. 2012;113:1294-1303.
64. Yano Y, Ning H, Reis JP, Lewis CE, Launer LJ, Bryan RN, Yaffe K, Sidney S, Albanese E, Greenland P, Lloyd-Jones D, Liu K. Blood pressure reactivity to psychological stress in young adults and cognition in midlife: the Coronary Artery Risk Development in Young Adults (CARDIA) Study. J Am Heart Assoc. 2016;5:e002718. DOI: 10.1161/JAHA.115.002718.
65. Matthews KA, Katholi CR, McCreath H, Whooley MA, Williams DR, Zhu S, Markovitz JH. Blood pressure reactivity to psychological stress predicts hypertension in the CARDIA study. Circulation. 2004;110:74-78.
66. Treiber FA, Kamarck T, Schneiderman N, Sheffield D, Kapuku G, Taylor T. Cardiovascular reactivity and development of preclinical and clinical disease states. Psychosom Med. 2003;65:46-62.
67. Gianaros PJ, Bleil ME, Muldoon MF, Jennings JR, Sutton-Tyrrell K, McCaffery JM, Manuck SB. Is cardiovascular reactivity associated with atherosclerosis among hypertensives? Hypertension. 2002;40:742-747.
68. Pires PW, Dams Ramos CM, Matin N, Dorrance AM. The effects of hypertension on the cerebral circulation. Am J Physiol Heart Circ Physiol. 2013;304:H1598-H1614.
69. Hajjar I, Goldstein FC, Martin GS, Quyyumi AA. Roles of arterial stiffness and blood pressure in hypertension-associated cognitive decline in healthy adults. Hypertension. 2016;67:171-175.
70. Pase MP, Himali JJ, Mitchell GF, Beiser A, Maillard P, Tsao C, Larson MG, DeCarli C, Vasan RS, Seshadri S. Association of aortic stiffness with cognition and brain aging in young and middle-aged adults: the Framingham Third Generation Cohort Study. Hypertension. 2016;67:513-519.
71. van Sloten TT, Protogerou AD, Henry RM, Schram MT, Launer LJ, Stehouwer CD. Association between arterial stiffness, cerebral small vessel disease and cognitive impairment: a systematic review and meta-analysis. Neurosci Biobehav Rev. 2015;53:121-130.
72. Raji CA, Eyre H, Wei SH, Bredesen DE, Moylan S, Law M, Smal G, Thompson PM, Friedlander RM, Silverman DH, Baune BT, Hoang TA, Salamon N, Toga AW, Vernooij MW. Hot topics in research: preventive neuroradiology in brain aging and cognitive decline. AJNR Am J Neuroradiol. 2015;36:1803-1809.
73. Villapol S, Saavedra JM. Neuroprotective effects of angiotensin receptor blockers. Am J Hypertens. 2015;28:289-299.
74. Faraco G, Iadecola C. Hypertension: a harbinger of stroke and dementia. Hypertension. 2013;62:810-817.
75. Iadecola C. Hypertension and dementia. Hypertension. 2014;64:3-5.