| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
(Stroke. 1996;27:1290-1295.)
© 1996 American Heart Association, Inc.
Articles |
Ultrasonographic Assessment of Carotid Wall Characteristics and Cognitive Functions in a Community Sample of 59- to 71-Year-Olds
INSERM U360, Hopital de la Salpetriere (A. Auperin, C.B., A. Alperovitch), INSERM U258, Hopital Broussais (C.B.-K., P.D.), and the Service de Neurologie, Hopital Saint Antoine (P.-J.T.), Paris; and Centre EVA (I.R.), Nantes, France.
Correspondence to C. Berr, INSERM U360, Hopital de la Salpetriere, 47 Blvd de l'Hopital, 75651 Paris Cedex 13, France.
 |
Abstract |
|---|
 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Background and Purpose This study was aimed at analyzing cross-sectional relationships between cognitive performance and ultrasonographic assessment of carotid wall characteristics.
Methods A cohort of 1279 subjects (men, 41%) aged 59 to 71 years was recruited from the electoral rolls of the city of Nantes (western France). Cognitive performances were evaluated with the Mini-Mental State Examination (MMSE) and seven neuropsychological tests assessing attention, psychomotor rapidity, verbal abilities, memory, and visuospatial perception. For each test, subjects were classified into three performance levels with a quartile distribution: 25% highest, 25% lowest, and 50% middle. The intima-media thickness of common carotid arteries and the presence of plaques in the carotid arteries were assessed with B-mode ultrasound examination.
Results Only 28% of men and 17% of women had carotid plaques inducing moderate stenosis of the lumen (<40%). After adjustment for possible confounders, odds ratios for poor cognitive performance associated with plaques were above 1 for all cognitive tests in men. This association was statistically significant for the MMSE and another test assessing attention skills. There was a slight association between increase of the common carotid intima-media thickness and poor cognitive scores in men with plaques. In women, no association was found between cognitive functions and presence of plaques or intima-media thickness.
Conclusions This study indicated a moderate association between atherosclerosis of the carotid arteries and poor cognitive functioning in men aged 59 to 71 years. In view of these moderate cross-sectional results, further studies are required to better assess the relationship between carotid atherosclerosis and cognitive impairment.
Key Words: aging • atherosclerosis • carotid arteries • cognition • epidemiology
|
Introduction |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
The prevalence of cognitive impairment increases with age, but among elderly individuals of the same age, some have normal cognitive functioning while others have a severe deterioration of their cognitive abilities. These interindividual differences are largely unexplained. Among the potential determinants of the importance of age-associated cognitive decline, recent studies have focused on atherosclerosis and its related risk factors. The relationship between blood pressure and cognitive function in the elderly remains uncertain.1 2 3 4 5 Very little is known about the relationship between cognitive functioning and other vascular risk factors. It has been suggested that diabetes and hypercholesterolemia are associated with an increased prevalence of specific cognitive deficits.6 In a population study of 4971 subjects aged 55 to 94 years, Breteler et al7 8 found that the presence of plaques in the carotid bifurcation and previous myocardial infarction were associated with low MMSE scores.
We examined cross-sectional relationships between cognitive functioning and carotid wall characteristics in a large population sample of individuals aged 59 to 71 years to determine whether carotid atherosclerotic lesions were associated with low cognitive performance.
|
Subjects and Methods |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Population
The EVA Study is a 4-year, ongoing, longitudinal study performed in volunteers aged 59 to 71 years recruited from the electoral rolls of the city of Nantes (western France). It was designed to investigate vascular and cognitive aging processes. It was approved by the Ethics Committee of the University Hospital of Bicetre, and written consent was given by each participant. Between June 1991 and July 1993, 1389 subjects were included and underwent baseline examination at the EVA Study center. Subjects with a history of stroke (n=30) were excluded from the present analysis.
Carotid Examination
A high-resolution B-mode ultrasound examination of left and right carotid arteries in 1385 subjects was performed using an Aloka SSD-650 with a 7.5-MHz transducer. Acquisition, processing, and storage of B-mode images were computer-assisted using a software specially designed for longitudinal studies.9 The ultrasound examination involved scanning the common carotid arteries, the carotid bifurcations, and the first 2 cm of the internal carotid arteries. The IMT (distance between the media-adventitia interface and the lumen-intima interface) was automatically measured twice on longitudinal B-mode images of the far wall of each common carotid artery at plaque-free sites. The common carotid IMT was defined as the mean of four measurements. All segments of the carotid arteries were scanned longitudinally and transversely to assess the presence of plaques, and a localized echo-structure protruding into the lumen was considered to be a plaque if the distance between the media-adventitia interface and the internal side of the lesion was 
1 mm. The total number of plaques was recorded. For each, maximum thickness was measured perpendicular to the vessel wall. When several plaques were present in the same carotid segment (ie, common carotid artery or bifurcation/origin of the internal carotid artery), plaque thickness measurement was made only for that with the greatest protrusion into the lumen. On the basis of transverse views, the degree of carotid stenosis was defined as (1-residual area/vessel area)x100%.
Interreader variations were analyzed in random subsamples of longitudinal images. Interreader agreement regarding the presence of plaques was excellent (
coefficient=.90). The correlation coefficient between repeated readings was .82 for IMT and .78 for plaque thickness. Because of technical reasons, the ultrasound examinations performed during the first weeks of the study were considered unreliable and were excluded (n=77).
Neuropsychological Testing
Subjects were evaluated with a neuropsychological battery that included seven tests assessing different cognitive functions and a global test (MMSE) of 18 items roughly assessing various cognitive skills with scores ranging from 0 to 30. An MMSE score <24 is considered indicative of poor cognitive skills.10 Visual attention and psychomotor rapidity were assessed with the TMT, part B, and the DSST from the Wechsler Intelligence Scale–Revised. Auditory attention was evaluated with the PASAT. The BVRT assessed visuospatial perception. The battery also included an assessment of immediate memory and learning strategies with the AVLT and of verbal fluency and search strategies with the WFT. General skills such as logical intelligence and reasoning were studied with the RPM. The MMSE, DSST, WFT, and RPM were administered to all participants. The other tests were administered to subjects who obtained an MMSE score 24. Six subjects with major sensorial inabilities were excluded.
Measurement of Covariates
The currently available literature suggests potential risk factors for poor cognitive functioning; these factors were measured and used in the analysis. Educational achievement was distributed in four categories based on years of schooling: 0 to 5, 6 to 9, 10 to 12, and >12. Subjects were also categorized as current smokers, former smokers, and nonsmokers. Weekly consumption of alcohol was determined, and three categories of average daily intake (in milliliters) were created: no alcohol consumption, 1 to 40 mL/d, and >40 mL/d.
Subjects completed the CES-D scale, a 20-item self-report of depressive symptoms presented during the week preceding the baseline examination.11 CES-D scores >16 in men and >22 in women are considered the cutoff levels for depression screening in the French population.12
Two independent measurements of systolic and diastolic blood pressure were taken with a digital electronic tensiometer after a 10-minute rest. The mean of the two measures was used in the analysis.
Statistical Analysis
Analysis was performed separately in men and women, using the SAS software package. For each cognitive test, three levels of cognitive performance were defined according to quartiles of test-score distribution: the lowest quartile defined a poor level, the highest a high level, and the two intermediate quartiles a middle level.
Bivariate associations were assessed with the 
2 test and variance analysis, and statistical testing of trends was performed when necessary. Nominal polychotomous logistic regressions13 (BMDP statistical software) were used to analyze the relationships between each cognitive score distribution of the eight neuropsychological tests and carotid characteristics (presence of plaques, IMT), adjusting for age, education, depressive symptomatology, systolic blood pressure, body mass index, smoking, and alcohol consumption. The cognitive performance was the explained variable. Because there were three cognitive performance levels, two odds ratios were computed for each carotid characteristic considered a potential risk factor for cognitive functioning; one contrasted poor versus high cognitive score categories and the other contrasted intermediate versus high cognitive score categories. For each odds ratio, the high cognitive level was the reference category.
|
Results |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
The sample consisted of 526 men and 753 women (mean age, 65.0±3.0 years) whose characteristics are given in Table 1
. The prevalence of plaques was higher in men (28%) than in women (17%). However, the severity of plaques was similar in men and women, with approximately 85% of plaques involving a carotid stenosis of <20% (Table 1). Common carotid IMT was lower in women than in men, but in both sexes, IMT was greater in those with plaques than in those without them.
|
Mean MMSE score was 28.3±2.0 in men versus 27.9±2.3 in women; 3.4% of men and 5.6% of women had MMSE scores <24. All cognitive scores were strongly associated with educational level in both sexes.
Crude relationships between plaques and cognitive functioning are shown in the Figure. In all cognitive tests, prevalence of carotid plaques was higher in men with poor cognitive performance than in those with high performance. A significant (P<.05) or borderline (P<.10) trend to an increasing prevalence of plaques from the high to the poor cognitive performance category was found in five of the eight neuropsychological tests: MMSE, DSST, TMT, PASAT, and AVLT. Thus, with the MMSE, the percentages of men with plaques in the poor, middle, and high score categories were 34.9%, 26.5%, and 25.0%, respectively. Moreover, in four tests, we found a significant trend (P<.05) to an increased number of plaques associated with decreasing cognitive performance (DSST and PASAT) or a borderline trend (P<.10; MMSE and TMT). In men with carotid plaques, there was no relationship between plaque thickness and cognitive functioning. Table 2 shows odds ratios and 95% confidence intervals with regard to carotid plaques in men, which were obtained from polychotomous logistic regression models. In all neuropsychological tests, the odds ratios related to carotid plaques for poor versus high cognitive performances were >1, but they were significant only with MMSE and DSST. The odds ratios for middle versus high cognitive performances were close to 1.0 in all neuropsychological tests but one (DSST), indicating that these two levels of performance were almost similar whether carotid plaques were present or not.
|
|
In women, no association, not even a trend, was found between cognitive performance and the presence or number of plaques (Figure
).
In men, we found no consistent relationship between common carotid IMT and cognitive functions (Table 3). In only two tests (DSST and WFT) was a statistically significant trend observed, since the mean IMT increased with high to poor cognitive performance levels. Separate analyses were performed in men with and without plaques. In men with plaques, significant or borderline associations between higher IMT and lower test scores were found for four of the eight tests. In men without plaques, no association was found. In men with plaques, estimates of odds ratios obtained from logistic regression models, with adjustment for possible confounders, also showed a slight increase in the risk of poor cognitive scores associated with a 0.1-mm increase in the common carotid IMT (Table 4).
|
|
In women, no relationship was observed between common carotid IMT and cognitive performance (Table 3).
|
Discussion |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
This study showed a consistent, moderate association in men aged 59 to 71 years between carotid plaques and poor cognitive performance, independent of the main potential confounders. The presence of plaques apparently affected all the cognitive functions assessed by the test battery. Moreover, in men with plaques, a slight positive correlation was suggested between common carotid IMT and risk of poor cognitive scores. In women, the level of cognitive functioning was associated neither with plaques nor with IMT.
Because the EVA cohort has a higher educational level and better cognitive scores than the French population of the same age,14 participation in the study was probably selective. Consequently, the contrast between high and poor cognitive levels defined according to quartiles of cognitive-score distribution was weak. Because the reproducibility of carotid measurements was good, the ultrasound measurement errors should only slightly have affected the relationship under study. The prevalence of plaques was low, and the mean IMT of the common carotid was below that reported for other elderly populations.15 16 17 With the number of subjects included in this study, the power of a two-tailed test (
=5%) was adequate in men and women (80%) to detect an odds ratio 2 for poor cognitive performance with plaques.
The association observed in men between carotid atherosclerosis and cognitive functioning was slight, but this is consistent with previous reports. In the Rotterdam study, Breteler et al7 8 found that, in individuals aged 75 to 94 years, plaques in the carotid bifurcation were significantly associated with low MMSE scores; this was not significant in individuals aged 55 to 74 years. In this cross-sectional analysis, peripheral arterial diseases and previous myocardial infarction assessed with electrocardiography were also associated with low MMSE scores. Two small longitudinal studies18 19 suggested that atherosclerotic diseases were a risk factor for cognitive decline.
In the present study, poor cognitive functioning was associated with plaques, whereas there was only a weak association with common carotid IMT in the subgroup of men with plaques. This may suggest that these two types of vascular lesions result from different pathophysiological mechanisms: atherosclerosis for plaques, and adaptive or aging-associated nonatheromatous process for intimal and medial thickening.20 21 22 Ultrasound studies, however, have indicated that intima-media thickening is associated with classic atherosclerosis risk factors such as age, hypertension, lipid alterations, or smoking.23 24 25 26 27 28 29 30 Thus, if a greater intima thickness is an early phase of the atherosclerotic process,31 it may be associated with no clinically observable disorders, especially for low values of the IMT such as those we measured. In the EVA study, age and systolic blood pressure were strongly correlated with both thicker intima-media and plaques, and an independent association between both types of carotid lesions was also found.32
Because atherosclerotic lesions led to low-grade carotid stenosis (<40% in all men but one), it is most unlikely that hemodynamic disturbances could explain cognitive impairment. In white matter lesions shown on MRI in elderly persons, pathological studies33 34 have described arteriolosclerosis, a degenerative disease of the smallest arteries. Recent studies found that white matter lesions were associated with increased carotid IMT, presence of plaques,35 36 and poor cognitive function.37 38 39 40 41 Since the association between carotid plaques and poor cognitive functioning persisted after adjustment for main vascular risk factors, other factors, such as angiotensin-converting enzyme, could affect both carotid arteries and intracerebral small arteries despite their histological difference.
In contrast to the results in men, we found no relationship between cognitive performances and carotid characteristics in women. The power of the study was not lower in women than in men. But it is well established that vascular diseases differ in men and women. First, the incidence of vascular morbidity is shifted to higher ages in women. The prevalence of carotid artery plaques is higher in men than in women of the same age,17 42 and the sex gap in morbidity due to coronary disorders tends to diminish only after 75 years of age.43 Second, the probabilities of vascular diseases attached to cardiovascular risk factors are not the same for men and women.17 43 The process that could explain the association observed in men between carotid atherosclerosis and cognitive functioning is unknown, and it could work differently in women. A gap in age or the absence of association in women are two possible hypotheses.
Further cross-sectional and longitudinal studies are needed to assess relationships between carotid artery disease, vascular risk factors, white matter lesions, and cognitive decline in the elderly.
|
Selected Abbreviations and Acronyms |
|---|
|
|
Acknowledgments |
|---|
The EVA Study Group is organized under an agreement between INSERM and Merck, Sharp, & Dohme–Chibret.
|
Footnotes |
|---|
Review of this manuscript was directed by Mark L. Dyken, MD.
Received November 24, 1995; revision received March 6, 1996; accepted April 12, 1996.
|
References |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
1. Wallace RB, Lemke JH, Morris MC, Goodenberger M, Kohout F, Hinrichs JV. Relationship of free-recall memory to hypertension in the elderly: the Iowa 65+ rural health study. J Chronic Dis. 1985;38:475-481.[Medline] [Order article via Infotrieve]
2. Farmer ME, Kittner SJ, Abbott RD, Wolz MM, Wolf PA, White LR. Longitudinally measured blood pressure, antihypertensive medication use, and cognitive performance: the Framingham study. J Clin Epidemiol. 1990;43:475-480.[Medline] [Order article via Infotrieve]
3.
Scherr PA, Hebert LE, Smith LA, Evans DA. Relation of blood pressure to cognitive function in the elderly. Am J Epidemiol. 1991;134:1303-1315.
4.
Elias MF, Wolf PA, D'Agostino RB, Cobb J, White LR. Untreated blood pressure level is inversely related to cognitive functioning: the Framingham study. Am J Epidemiol. 1993;138:353-364.
5. Breteler MMB. Blood pressure, hypertension, orthostatic hypotension, and cognitive function in the elderly. Cognitive Decline in the Elderly. Rotterdam, Netherlands: Erasmus University; 1993:86-98. Thesis.
6.
Desmond DW, Tatemichi TK, Paik M, Stern Y. Risk factors for cerebrovascular disease as correlates of cognitive function in a stroke-free cohort. Arch Neurol. 1993;50:162-166.
7.
Breteler MMB, Claus JJ, Grobbee DE, Hofman A. Cardiovascular disease and distribution of cognitive function in elderly people: the Rotterdam study. BMJ. 1994;308:1604-1608.
8. Breteler MMB. Atherogenic and hemostatic factors and cognitive function in the elderly. Cognitive Decline in the Elderly. Rotterdam, Netherlands: Erasmus University; 1993:74-85. Thesis.
9. Touboul PJ, Prati P, Scarabin PY, Adrai V, Thibout E, Ducimetiere P. Use of monitoring software to improve the measurement of carotid wall thickness by B-mode imaging. J Hypertens. 1992;10(suppl 5):S37-S41.
10. Folstein MF, Folstein SE, MacHugh PR. `Mini-Mental State': a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189-198.[Medline] [Order article via Infotrieve]
11. Radloff LS. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1:385-401.
12. Fuhrer R, Rouillon F. La version francaise de l'echelle CES-D (Center for Epidemiologic Studies–Depression Scale): description et traduction de l'echelle d'auto-evaluation. Psychiatr Psychobiol. 1989;4:163-166.
13. Hosmer DW, Lemeshow S. Polytomous logistic regression. In: Applied Logistic Regression. New York, NY: John Wiley & Sons Inc; 1989:216-238.
14. Dealberto MJ, Gagnon M, Baberger-Gateau P, Dartigues JF, Alperovitch A. Influence of the education level on a screening test for dementia, the Mini-Mental State Examination. Rev Epidemiol Sante Publique. 1992;40:93-101.[Medline] [Order article via Infotrieve]
15. Josse MO, Touboul PJ, Mas JL, Laplane D, Bousser MG. Prevalence of asymptomatic internal carotid artery stenosis. Neuroepidemiology. 1987;6:150-152.[Medline] [Order article via Infotrieve]
16.
Prati P, Vanuzzo D, Casaroli M, Di Chiara A, De Biasi F, Feruglio GA, Touboul PJ. Prevalence and determinants of carotid atherosclerosis in a general population. Stroke. 1992;23:1705-1711.
17.
Willeit J, Kiechl S. Prevalence and risk factors of asymptomatic extracranial carotid artery atherosclerosis: a population-based study. Arterioscler Thromb. 1993;13:661-668.
18. Hertzog C, Schaie KW, Gribbin K. Cardiovascular disease and changes in intellectual functioning from middle to old age. J Gerontol. 1978;33:872-883.
19. Poitrenaud J, Vallery-Masson J, Darcet P, Barrere H, Derriennic F, Guez D. Sources of individual differences in cognitive aging: a longitudinal study of an elderly French managerial population. Annee Gerontol/Facts and Research in Gerontology. 1994;8:462-477.
20. Glagov S, Zarins CK. Is intimal hyperplasia an adaptative response or a pathologic process? Observations on the nature of nonatherosclerotic intimal thickening. J Vasc Surg. 1989;10:571-573.
21.
Chobanian AV. 1989 Corcoran lecture: adaptative and maladaptative responses of the arterial wall to hypertension. Hypertension. 1990;15:666-674.
22. Wei JY. Age and the cardiovascular system. N Engl J Med. 1992;327:1735-1739.[Medline] [Order article via Infotrieve]
23. Salonen R, Salonen JT. Progression of carotid atherosclerosis and its determinants: a population-based ultrasonography study. Atherosclerosis. 1990;81:33-40.[Medline] [Order article via Infotrieve]
24.
Bonithon-Kopp C, Scarabin PY, Taquet A, Touboul PJ, Malmejac A, Guize L. Risk factors for early carotid atherosclerosis in middle-aged French women. Arterioscler Thromb. 1991;11:966-972.
25.
Heiss G, Sharrett AR, Barnes R, Chambless LE, Szklo M, Alzola C, for the ARIC investigators. Carotid atherosclerosis measured by B-mode ultrasound in populations: associations with cardiovascular risk factors in the ARIC Study. Am J Epidemiol. 1991;134:250-256.
26. Salonen R, Salonen JT. Determinants of carotid intima-media thickness: a population-based ultrasonography study in Eastern Finnish men. J Intern Med. 1991;229:225-231.[Medline] [Order article via Infotrieve]
27.
Psaty BM, Furberg CD, Kuller LH, Borhani NO, Rautaharju PM, O'Leary DH, Bild DE, Robbins J, Fried LP, Reid C. Isolated systolic hypertension and subclinical cardiovascular disease in the elderly: initial findings from the Cardiovascular Health Study. JAMA. 1992;268:1287-1291.
28.
Bots ML, Hofman A, De Bruyn AM, De Jong PTVM, Grobbee DE. Isolated systolic hypertension and vessel wall thickness of the carotid artery: the Rotterdam Elderly Study. Arterioscler Thromb. 1993;13:64-69.
29.
Sharrett AR, Patsch W, Sorlie PD, Heiss G, Bond MG, Davis CE, for the ARIC Investigators. Associations of lipoprotein cholesterols, apolipoproteins A-I and B, and triglycerides with carotid atherosclerosis and coronary heart disease: the Atherosclerosis Risk in Communities Study. Arterioscler Thromb. 1994;14:1098-1104.
30.
Lemne C, Jogestrand T, De Faire U. Carotid intima-media thickness and plaque in borderline hypertension. Stroke. 1995;26:34-39.
31.
Stary HC, Blankenhorn DH, Chandler AB, Glagov S, Insull W Jr, Richardson M, Rosenfeld ME, Schaffer SA, Schwartz CJ, Wagner WD, Wissler RW. A definition of the intima of human arteries and of its atherosclerosis-prone regions. Arterioscler Thromb. 1992;12:120-134.
32.
Bonithon-Kopp C, Touboul PJ, Berr C, Leroux C, Mainard F, Courbon D, Ducimetiere P. Relation of intima-media thickness to atherosclerotic plaques in the carotid arteries: the EVA study. Atheroscler Thromb Vasc Biol. 1996;16:310-316.
33.
Revesz T, Hawkins CP, Du Boulay EPGH, Barnard RO, MacDonald WI. Pathological findings correlated with magnetic resonance imaging in subcortical arteriosclerotic encephalopathy. J Neurol Neurosurg Psychiatry. 1989;52:1337-1344.
34.
Van Swieten JC, Van Den Hout JHW, Van Ketel BA, Hijdra A, Wokke JHJ, Van Gijn J. Periventricular lesions in the white matter on magnetic resonance imaging in the elderly: a morphometric correlation with arteriolosclerosis and dilated perivascular spaces. Brain. 1991;114:761-774.
35. Bots ML, Van Swieten JC, Breteler MMB, De Jong PTVM, Van Gijn J, Hofman A, Grobbee DE. Cerebral white matter lesions and atherosclerosis in the Rotterdam study. Lancet. 1993;341:1232-1237.[Medline] [Order article via Infotrieve]
36. Manolio TA, Kronmal RA, Burke GL, Poirier V, O'Leary DH, Gardin JM, Fried LP, Steinberg EP, Bryan RN, for the Cardiovascular Health Study Collaborative Research Group. Magnetic resonance abnormalities and cardiovascular disease in older adults: the Cardiovascular Health Study. Stroke. 1994;25:318-327.[Abstract]
37.
Junque C, Pujol J, Vendrell P, Bruna A, Jodar M, Ribas JC, Vinas J, Capdevila A, Marti-Vilalta JL. Leuko-araiosis on magnetic resonance imaging and speed of mental processing. Arch Neurol. 1990;47:151-156.
38.
Boone KB, Miller BL, Lesser IM, Mehringer CM, Hill-Gutierrez E, Goldberg MA, Berman NG. Neuropsychological correlates of white-matter lesions in healthy elderly subjects. Arch Neurol. 1992;49:549-554.
39.
Matsubayashi K, Shimada K, Kawamoto A, Ozawa T. Incidental brain lesions on magnetic resonance imaging and neurobehavioral functions in the apparently healthy elderly. Stroke. 1992;23:175-180.
40. Breteler MMB, Van Amerongen NM, Van Swieten JC, Claus JJ, Grobbee DE, Van Gijn J, Hofman A, Van Harskamp F. Cognitive correlates of ventricular enlargement and cerebral white matter lesions on magnetic resonance imaging: the Rotterdam Study. Stroke. 1994;25:1109-1115.[Abstract]
41.
Breteler MMB, Van Swieten JC, Bots ML, Grobbee DE, Claus JJ, Van Den Hout JHW, Van Harskamp F, Tanghe HLJ, De Jong PTVM, Van Gijn J, Hofman A. Cerebral white matter lesions, vascular risk factors and cognitive function in a population-based study: the Rotterdam Study. Neurology. 1994;44:1246-1252.
42.
O'Leary DH, Polak JF, Kronmal RA, Kittner SJ, Bond MG, Wolfson SK, Bommer W, Price TR, Gardin JM, Savage PJ, for the CHS Collaborative Research Group. Distribution and correlates of sonographically detected carotid artery disease in the Cardiovascular Health Study. Stroke. 1992;23:1752-1760.
43. Lerner DJ, Kannel WB. Patterns of coronary heart disease morbidity and mortality in the sexes: a 26-year follow-up of the Framingham population. Am Heart J. 1986;111:383-390.[Medline] [Order article via Infotrieve]
This article has been cited by other articles:
 |
|
 |
|
  M. de Weerd, J. P. Greving, A. W.F. de Jong, E. Buskens, and M. L. Bots Prevalence of Asymptomatic Carotid Artery Stenosis According to Age and Sex: Systematic Review and Metaregression Analysis Stroke, April 1, 2009; 40(4): 1105 - 1113. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. J. Smith, J. A. Blumenthal, M. A. Babyak, B. M. Hoffman, P. M. Doraiswamy, R. Waugh, A. Hinderliter, and A. Sherwood Cerebrovascular Risk Factors, Vascular Disease, and Neuropsychological Outcomes in Adults With Major Depression Psychosom Med, July 1, 2007; 69(6): 578 - 586. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Dufouil, F. Richard, N. Fievet, J. F. Dartigues, K. Ritchie, C. Tzourio, P. Amouyel, and A. Alperovitch APOE genotype, cholesterol level, lipid-lowering treatment, and dementia: The Three-City Study Neurology, May 10, 2005; 64(9): 1531 - 1538. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. B. Mathiesen, K. Waterloo, O. Joakimsen, S. J. Bakke, E. A. Jacobsen, and K. H. Bonaa Reduced neuropsychological test performance in asymptomatic carotid stenosis: The Tromso Study Neurology, March 9, 2004; 62(5): 695 - 701. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. R. Waldstein, C. F. Tankard, K. J. Maier, J. R. Pelletier, J. Snow, A. W. Gardner, R. Macko, and L. I. Katzel Peripheral Arterial Disease and Cognitive Function Psychosom Med, September 1, 2003; 65(5): 757 - 763. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. M. Fillit, R. N. Butler, A. W. O'Connell, M. S. Albert, J. E. Birren, C. W. Cotman, W. T. Greenough, P. E. Gold, A. F. Kramer, L. H. Kuller, et al. Achieving and Maintaining Cognitive Vitality With Aging Mayo Clin. Proc., July 1, 2002; 77(7): 681 - 696. [Abstract] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||