Executive function in systemic arterial hypertension: A systematic review

Moraes, Natália Cristina; Aprahamian, Ivan; Yassuda, Mônica Sanches

doi:10.1590/1980-57642018dn13-030004

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Dementia & Neuropsychologia

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Original Article • Dement. neuropsychol. 13 (3) • Jul-Sep 2019 • https://doi.org/10.1590/1980-57642018dn13-030004 copy

Executive function in systemic arterial hypertension: A systematic review

FUNÇÃO EXECUTIVA NA HIPERTENSÃO ARTERIAL SISTÊMICA: UMA REVISÃO SISTEMÁTICA

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Systemic arterial hypertension (SAH) may be associated with worse cognitive performance, especially in tasks that evaluate the executive functions (EF).

Objective:

we aimed to review the evidence regarding which components of executive functions are most affected in adults with SAH.

Methods:

this systematic review used the PRISMA statement for searching Pubmed, Scielo and Lilacs databases with the keywords “executive function OR executive functioning AND hypertension”.

Results:

EF tasks were divided into shifting, inhibitory control and updating. A total of 9 cross-sectional and 3 longitudinal studies were selected. Only 3 studies did not report worse performance among SAH patients on EF tasks when compared to normotensive controls. The measures of shifting and inhibitory control were the most frequently investigated and reported as altered among SAH individuals, assessed mainly by the Stroop Test and Trail-Making Test part B, respectively.

Conclusion:

inhibitory control and shifting are the EF components most influenced by SAH. The results of this review may contribute to the devising of hypotheses about mechanisms underlying these cognitive impairments.

Key words:
hypertension; executive functions; cognition; systematic review

EF component	Neuropsychological task	Cognitive demand
Inhibitory control	Stroop Test¹⁹19 MacLeod CM. Half a century of research on the Stroop effect: an integrative review. Psychol Bull.1991;109:163-203.	Names of colors (e.g. "green") printed in a different color (e.g. "red"), where it is necessary to inhibit the reading of the word to report the color of the ink.
Inhibitory control	Go-no-go tasks⁹9 Diamond A. Executive functions. Ann Rev Psychol. 2013;64:135-68.	This type of task requires the subject to inhibit one response in favor of another, such as pressing a button when a stimulus appears, and not pressing when a different stimulus appears.
Updating	Digit Span Backwards²⁰20 Nascimento E. Adaptação, validação e normatização do WAIS-III para uma amostra brasileira. In: Wescheler D. WAIS-III manual para administração e avaliação. São Paulo, Casa do Psicólogo; 2004.	Requires the subject to repeat a sequence of numbers backwards. The numbers must be retained mentally and worked with simultaneously.
	Verbal Fluency²¹21 Lezak MD, Howieson DB, Loring DW. Neuropsychological assessment (4th ed.). New York: Oxford University Press; 2004.	The subject has to utter as many words as they can in the same semantic or phonemic order within sixty seconds.
	Reorder Items⁹9 Diamond A. Executive functions. Ann Rev Psychol. 2013;64:135-68.	The subject is asked to reorder names of animals or numbers by increasing size.
Shifting	Trail-Making Test part B²²22 Arbuthnott K and Frank J. Trail Making Test, Part B as a Measure of Executive Control: Validation Using a Set-Switching Paradigm. J Clin Exp Neuropsychol. 2000;22:518-28.	The subject needs to connect numbers and letters, alternating them with numbers in ascending order and letters in alphabetical order as fast as they can.
Shifting	Wisconsin Card Sorting Task²³23 Stuss DT, Levine B, Alexander MP, Hong J, Palumbo C, Hamer L, et al. Wisconsin Card Sorting Test performance in patients with focal frontal and posterior brain damage: Effects of lesion location and test structure on separable cognitive processes. Neuropsychology. 2000;38:388-402.	Each card can be classified by color, shape or number. The subject must deduce the classification criteria based on feedback provided by the examiner and shifting the classification rules whenever needed.

Study	Country	Sample	Education (years)	Gender distribution	Diagnosis time	Follow-up time
Cross-sectional
Waldstein et al., 1996²⁶26 Waldstein SR, Jennings JR, Ryan C., Muldoon MF, Shapiro AP, Polefrone JM. Hypertension and neuropsychological performance in men: Interactive effects of age. Health Psychol 1996;15(2):102-9.	USA	Hypertensive and normotensive young and middle-aged	9-21 years	Only men	N/A
Kuo et al., 2004²⁷27 Kuo HK, Sorond F, Iloputaife I, Gangon M, Milberg W, Lipsitz LA. Effect of blood pressure on cognitive functions in elderly persons. J Gerontol A Biol Sci Med Sci. 2004;59:1191-4.	USA	Normotensive and hypertensive	12-20 years	44.3% women	N/A
Vicario et al., 2005²⁸28 Vicario A, Martinez CD, Baretto D, Diaz Casale A, Nicolosi L. Hypertension and cognitive decline: Impact on executive function. J Clin Hypertens. 2005;7(10):598-604.	Argentina	Normotensive and hypertensive	4-11 years	62.2% women	5-30 years
Hannesdottir et al., 2009²⁹29 Hannesdottir K, Nitkunan A, Charlton RA, Barrick TR, MacGregor GA, Markus HS. Cognitive Impairment and White Matter Damage in Hypertension: A Pilot Study. Acta Neurol Scand. 2009;119(4):261-8.	England	Treated and untreated hypertensive and normotensive	<8 and >12 years	56.25% men	6 months-33 years
Bucur & Maden, 2010³⁰30 Buccur B, Madden DJ. Effects of Adult Age and Blood Pressure on Executive Function and Speed of Processing. Exp Aging Res, 2010; 36(2):153-68.	EUA	Normotensive and hypertensive	12-19 years	52.9% women	N/A
Giordano et al., 2012³¹31 Giordano N, Tikhonoff V, Palatini P, Bascelli A, Boschetti G, Lazzari F, et al. Cognitive Functions and Cognitive Reserve in Relation to Blood Pressure Components in a Population-Based Cohort Aged 53 to 94 Years. Int J Hypertens. 2012;2012:274851.	Italy	Normotensive and hypertensive	2-18 years	57% women	N/A
Matoso et al., 2013³²32 Matoso JMD, Santos WB, Moreira IFH, Lourenço RA, Correia MLG. Idosos Hipertensos apresentam menor desempenho cognitive do que idosos normotensos. Arq Bras Cardiol. 2013;100(5):444-51.	Brazil	Normotensive and hypertensive	7-12 years	53% women	N/A
Alipour et al., 2015³³33 Alipour H, Goldust M. The association between blood pressure components and cognitive functions and cognitive reserve. Clin Exp Hypertens. 2016;38:95-9.	Iran	Normotensive and hypertensive	3-10 years	54% women	N/A
Li et al., 2015³⁴34 Li X, Liang Y, Chen Y, Zhang J, Wei D, Chen K, et al. Disrupted Frontoparietal Network Mediates White Matter Structure Dysfunction Associated with Cognitive Decline in Hypertension Patients. J Neurosci. 2015;8;35(27):10015-24.	China	Normotensive and hypertensive	7-15 years	61.7% women	N/A
Longitudinal
Yasar et al., 2011³⁵35 Yasar S, Ko JY, Nothelle S, Mieke MM, Carlson M. Evaluation of the effect of Systolic Blood Pressure and Pulse Pressure on Cognitive Function: The Women's Health and Aging Study II. Plos One 2011;(6):12;e27976.	USA	Normotensive and hypertensive stages I and II	<12 and >12 years	N/A	N/A	9 years
Vicario et al., 2011³⁵35 Yasar S, Ko JY, Nothelle S, Mieke MM, Carlson M. Evaluation of the effect of Systolic Blood Pressure and Pulse Pressure on Cognitive Function: The Women's Health and Aging Study II. Plos One 2011;(6):12;e27976.	Argentina	Hypertensive	4-11 years	65% women	N/A	6 years
Chen et al., 2015³⁷37 Chen KHM, Hederson VW, Stolwyk RJ, Dennerstein L, Szoeke C. Prehypertension in midlife is associated with worse cognition a decade later in middle-aged and older women. Age and Aging. 2015;44:439-45.	Australia	Normotensive, pre-hypertensive and hypertensive	9-14 years	Only women	N/A	10 years

Authors, year of publication	Objective	Sample	EF tasks	Main results
Waldstein et al., 1996²⁶26 Waldstein SR, Jennings JR, Ryan C., Muldoon MF, Shapiro AP, Polefrone JM. Hypertension and neuropsychological performance in men: Interactive effects of age. Health Psychol 1996;15(2):102-9.	To investigate the interaction between age and hypertension on performance on neuropsychological tests. In this study, pharmacological treatment was discontinued two weeks before cognitive evaluation.	N=173; the groups were divided into young (≤40 years) and middle-aged (≥40 years), hypertensive and normotensive, totaling 4 groups.	Digit Span of the WAIS-II Scale, Phonemic Verbal Fluency, TMT part B and Stroop Test.	The young hypertensive group showed a significantly lower performance than the normotensive on the Stroop test, demonstrating worse inhibitory control. There was no difference between the middle age groups.
Kuo et al., 2004²⁷27 Kuo HK, Sorond F, Iloputaife I, Gangon M, Milberg W, Lipsitz LA. Effect of blood pressure on cognitive functions in elderly persons. J Gerontol A Biol Sci Med Sci. 2004;59:1191-4.	To determine the relationship between BP and different cognitive domains, and to analyze the relationship between decreased orthostatic pressure and cognitive functions in a relatively healthy elderly group.	N=70; ≥65 years old, elderly with stable chronic hypertension.	TMT part B and Verbal Fluency (Phonemic and Semantic).	Higher BP was associated with impairment in shifting performance as measured by TMT part B. Every 10 mmHg increase in systolic blood pressure (SBP) was associated with a 2.31 fold increase in the risk of impairment on this test.
Vicario et al., 2005²⁸28 Vicario A, Martinez CD, Baretto D, Diaz Casale A, Nicolosi L. Hypertension and cognitive decline: Impact on executive function. J Clin Hypertens. 2005;7(10):598-604.	To identify the effect of SAH on cognition and to differentiate this effect from other deterioration processes expected in aging.	N=90. There were 60 hypertensive and 30 normotensive aged ≥65 years.	Verbal and visual versions of TMT part B and Stroop Test.	The hypertensive subjects had more deficits on TMT part B, measure of shifting, with greater number of errors. The same group also exhibited deficits in IC performance, as measured by the Stroop Test.
Hannesdottir et al., 2009²⁹29 Hannesdottir K, Nitkunan A, Charlton RA, Barrick TR, MacGregor GA, Markus HS. Cognitive Impairment and White Matter Damage in Hypertension: A Pilot Study. Acta Neurol Scand. 2009;119(4):261-8.	The hypertensive subjects had more deficits on TMT part B, measure of shifting, with greater number of errors. The same group also revealed deficits in IC performance, as measured by the Stroop Test.	N=80; ≥59 years, 40 subjects treated, 10 untreated and 30 controls (normotensive).	Digit Span of WAIS III Scale, TMT part B and Verbal Fluency (Phonemic and Semantic).	Compared with the normotensive subjects, the untreated hypertensive group had worse performance on the Verbal Phonemic Fluency test, used for evaluating updating and IC.
Bucur & Madden, 2010³⁰30 Buccur B, Madden DJ. Effects of Adult Age and Blood Pressure on Executive Function and Speed of Processing. Exp Aging Res, 2010; 36(2):153-68.	To develop a more precise definition of the cognitive differences between hypertensive and normotensive.	N=131, 71 normotensive and 58 hypertensive individuals, categorized into young (19-39 years), middle age (41-58 years) and elderly (60-79 years).	Stroop Test, TMT part B and Phonemic Verbal Fluency.	The group of older hypertensive patients had worse performance than normotensive patients of the same age group on all EF tests, indicating impairment of IC, updating and shifting.
Giordano et al., 2012³¹31 Giordano N, Tikhonoff V, Palatini P, Bascelli A, Boschetti G, Lazzari F, et al. Cognitive Functions and Cognitive Reserve in Relation to Blood Pressure Components in a Population-Based Cohort Aged 53 to 94 Years. Int J Hypertens. 2012;2012:274851.	To investigate the relationship of different components of BP with cognitive functioning and cognitive reserve in a sample and identify which domains are most affected.	N=288, of which 234 were hypertensive and 54 normotensive aged ≥50 years.	TMT part B and Phonemic Verbal Fluency.	There was no difference between the hypertensive and normotensive groups in relation to the EF test performance.
Matoso et al., 2013³²32 Matoso JMD, Santos WB, Moreira IFH, Lourenço RA, Correia MLG. Idosos Hipertensos apresentam menor desempenho cognitive do que idosos normotensos. Arq Bras Cardiol. 2013;100(5):444-51.	To compare the cognitive performance of hypertensive and normotensive elderly with at least 5 years of education.	N=45, 17 normotensive and 28 hypertensive patients aged ≥60 years and <80 years.	TMT part B.	Hypertensive patients were significantly slower than normotensive patients. There was also a difference in the performance of the hypertensive group on TMT part B when compared to the normotensive group, indicating shifting impairment.
Alipour and Goldust, 2015³³33 Alipour H, Goldust M. The association between blood pressure components and cognitive functions and cognitive reserve. Clin Exp Hypertens. 2016;38:95-9.	To assess the relationship between BP measurements (SBP, DBP and PP) and cognitive functions and cognitive reserve.	N=500, with 248 hypertensive and 252 normotensive patients, aged ≥62 years.	TMT part B and Phonemic Verbal Fluency.	There was no significant difference in EF measurements between the groups.
Li et al., 2015³⁴34 Li X, Liang Y, Chen Y, Zhang J, Wei D, Chen K, et al. Disrupted Frontoparietal Network Mediates White Matter Structure Dysfunction Associated with Cognitive Decline in Hypertension Patients. J Neurosci. 2015;8;35(27):10015-24.	To evaluate the cognitive performance of hypertensive individuals in a large sample of ethnic Han people (China).	N=1007, of which 405 were hypertensive and 602 normotensive, aged 57-70 years.	TMT part B and Stroop test.	The hypertensive subjects had worse performance on the tests that evaluated IC and shifting when compared with normotensive controls.

Authors, year of publication	Objective	Sample	EF tasks	Main results
Yasar et al., 2011³⁵35 Yasar S, Ko JY, Nothelle S, Mieke MM, Carlson M. Evaluation of the effect of Systolic Blood Pressure and Pulse Pressure on Cognitive Function: The Women's Health and Aging Study II. Plos One 2011;(6):12;e27976.	To evaluate SBP or PP and cognitive impairment of elderly women over 9 years.	N=336, 103 normotensive, 124 hypertensive patients with SBP=140-159 mmHg and 109 hypertensive patients with SBP values ≥160 mmHg, aged 70-80 years.	TMT part B.	The HTN II had a five-fold increased risk of impairment on TMT part B, a measure of shifting, when compared to the normotensive group.
Vicario et al., 2011³⁶36 Vicario A, Sueldo MD, Zilberman JM, Cerezo GH. Cognitive Evolution in Hypertensive Patients: a six-year follow-up. Vasc Health Risk Manag. 2011;7:281-5.	To observe the cognitive evolution of hypertensive patients over 6 years.	N=60, hypertensive patients aged ≥68 years.	TMT part B and Stroop Test.	At 6 years of follow-up, there was decline in shifting (TMT part B) and inhibitory control (Stroop test).
Chen et al., 2015³⁷37 Chen KHM, Hederson VW, Stolwyk RJ, Dennerstein L, Szoeke C. Prehypertension in midlife is associated with worse cognition a decade later in middle-aged and older women. Age and Aging. 2015;44:439-45.	To examine the associations between BP levels and cognition in middle-aged and older women over 10 years.	N=247; the groups were divided into normotensive (91), pre-hypertensive (108) and hypertensive (48), divided into middle-aged and older women.	TMT part B.	There was no significant difference between the groups, both in the initial and follow-up analyses.

Studies	DF	PVF	SVF	Stroop Test	TMT B
Waldestein et al., 1996²⁶26 Waldstein SR, Jennings JR, Ryan C., Muldoon MF, Shapiro AP, Polefrone JM. Hypertension and neuropsychological performance in men: Interactive effects of age. Health Psychol 1996;15(2):102-9.	0	0	0	X	0
Kuo et al., 2004²⁷27 Kuo HK, Sorond F, Iloputaife I, Gangon M, Milberg W, Lipsitz LA. Effect of blood pressure on cognitive functions in elderly persons. J Gerontol A Biol Sci Med Sci. 2004;59:1191-4.		0	0		X
Vicario et al., 2005²⁸28 Vicario A, Martinez CD, Baretto D, Diaz Casale A, Nicolosi L. Hypertension and cognitive decline: Impact on executive function. J Clin Hypertens. 2005;7(10):598-604.				X	X
Hannesdottis et al., 2009²⁹29 Hannesdottir K, Nitkunan A, Charlton RA, Barrick TR, MacGregor GA, Markus HS. Cognitive Impairment and White Matter Damage in Hypertension: A Pilot Study. Acta Neurol Scand. 2009;119(4):261-8.	0	X			X
Bucur and Madden, 2010³⁰30 Buccur B, Madden DJ. Effects of Adult Age and Blood Pressure on Executive Function and Speed of Processing. Exp Aging Res, 2010; 36(2):153-68.		X		X	X
Giordano et al., 2012³¹31 Giordano N, Tikhonoff V, Palatini P, Bascelli A, Boschetti G, Lazzari F, et al. Cognitive Functions and Cognitive Reserve in Relation to Blood Pressure Components in a Population-Based Cohort Aged 53 to 94 Years. Int J Hypertens. 2012;2012:274851.		0			0
Matoso et al., 2013³²32 Matoso JMD, Santos WB, Moreira IFH, Lourenço RA, Correia MLG. Idosos Hipertensos apresentam menor desempenho cognitive do que idosos normotensos. Arq Bras Cardiol. 2013;100(5):444-51.					X
Alipour & Goldust, 2015³³33 Alipour H, Goldust M. The association between blood pressure components and cognitive functions and cognitive reserve. Clin Exp Hypertens. 2016;38:95-9.		0		0	0
Li et al., 2015³⁴34 Li X, Liang Y, Chen Y, Zhang J, Wei D, Chen K, et al. Disrupted Frontoparietal Network Mediates White Matter Structure Dysfunction Associated with Cognitive Decline in Hypertension Patients. J Neurosci. 2015;8;35(27):10015-24.				X	X

Studies	Stroop Test	TMTB
Yasar et al., 2011³⁵35 Yasar S, Ko JY, Nothelle S, Mieke MM, Carlson M. Evaluation of the effect of Systolic Blood Pressure and Pulse Pressure on Cognitive Function: The Women's Health and Aging Study II. Plos One 2011;(6):12;e27976.		X
Vicario et al., 2011³⁶36 Vicario A, Sueldo MD, Zilberman JM, Cerezo GH. Cognitive Evolution in Hypertensive Patients: a six-year follow-up. Vasc Health Risk Manag. 2011;7:281-5.	X	X
Chen et al., 2015³⁷37 Chen KHM, Hederson VW, Stolwyk RJ, Dennerstein L, Szoeke C. Prehypertension in midlife is associated with worse cognition a decade later in middle-aged and older women. Age and Aging. 2015;44:439-45.		0

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E-mail: revistadementia@abneuro.org.br | demneuropsy@uol.com.br

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[1] Natália Cristina Moraes. Neurology Department / Faculty of Medicine of the University of São Paulo - Av. Dr. Enéas Carvalho de Aguiar, 155 - 05403-000 São Paulo SP - Brazil. E-mail: moraes.na@gmail.com