[Frontiers in Bioscience E2, 980-990, June 1, 2010]
Carotid artery intima media thickness: a predictor of cognitive impairment?
TABLE OF CONTENTS
1. ABSTRACT
The conversion rate of cognitive impairment to Alzheimer's disease is 1 to 25% per year. Early detection of cognitive impairment will thus become a major concern, particularly when pharmacological intervention for preventing or delaying conversion will prove effective. If simple carotid artery intima media thickness (IMT) measurements were to predict cognitive impairment, IMT could become one of the detection tools, as it is inexpensive, reliable and non-invasive. Since no review paper on this subject is available, a systematic review of the literature was performed. Twenty studies were identified evaluating the association between IMT and cognitive impairment and fourteen found a significant association after multivariate analysis. However, currently no definitive evidence of an association between increased IMT and cognitive impairment can be established. A consensus regarding the precise definition of cognitive impairment, and standardized methods to assess early cognitive impairment alongside a consensus for IMT measurement are needed in future epidemiological studies on the relationship between IMT and cognitive impairment.
2. INTRODUCTION
Intima media thickness (IMT) of the common carotid artery (CCA) is increasingly considered as a marker for early atherosclerosis (10, 11, 42, 47) and vascular diseases, such as stroke, myocardial infarction and peripheral arterial disease (10, 47, 48). Atherosclerosis has been associated with dementia (29) and increased IMT values of the CCA have been correlated with parenchymal changes of the brain observed in dementia, such as leukoaraiosis (12,13, 66), making IMT a potential risk marker of cognitive impairment. However, the specific relationship between IMT and cognitive impairment remains poorly understood. Since no review paper on this subject is available, a systematic review of the literature was performed.
3. METHODS
A PubMed search from 1980 to 2009 was conducted. Key words were "intima-media thickness", "IMT", "wall thickness", "carotid atherosclerosis", "carotid stenosis" used in combined search with "neuropsychological test", "dementia", "cognitive impairment", "cognition", "cognitive decline" and "Alzheimer". The author aimed to select studies that evaluated the correlation between IMT and cognitive impairment. The electronic search resulted in 155 studies, of which 17 studies fulfilled the selection criteria. Three additional studies were identified through a manual search of retrieved references. All studies were subsequently classified and tabulated according to study design, patient demographics, IMT measurement methods, cognitive impairment criteria, as well as applied methods for cognitive assessment. In this review, 12 studies were cross-sectional (4-7, 60, 61, 63, 67-70, 72), four longitudinal (2, 3, 8, 9) population-based investigations, and four were both cross-sectional and longitudinal (1, 62, 65, 71).
4. RESULTS
4.1. Inclusion and exclusion criteria
Inclusion and exclusion criteria among studies varied to a high extent (Table 1). As increased IMT values were associated with stroke (47, 51), and stroke was correlated with cognitive impairment (29, 53-59), stroke might be a confounding factor. Therefore, studies reporting on IMT were distinguished primarily between post-stroke investigations and stroke-free investigations. Two studies (2, 9) considered stroke or transient ischemic attack (TIA) as their inclusion criteria. Twelve studies specified stroke as an exclusion criteria (1, 3-5, 61, 62, 65, 67-70,72). Other exclusion criteria were Parkinson's disease (2), Alzheimer's disease (2, 60), neoplasia (7, 60, 62), aphasia (2, 9), hypertension (60), dementia (62, 67), fasting total plasma homocysteine (Hcy) < 8.5 �mol/L (69) and ischemic heart disease (60). Three studies (6, 8, 71) did not report on this aspect.
4.2. Cognitive decline and cognitive impairment definitions
Definitions and assessment tools of cognitive decline and impairment varied across studies (Table 2). For screening purposes most frequently the Mini-Mental-Status Examination (MMSE) was used (1, 2, 4-6, 8, 9, 60, 62, 63, 65, 68, 70, 72). In addition to MMSE a variety of cognitive function assessment tools were applied, among which were the Digit Symbol Substitution Test (1, 4), the Montgomery-Asberg Depression Rating Scale (2) and the Dementia Rating Scale (5, 68). The majority of studies used an MMSE cut off score of twenty-four or less as indicative of cognitive impairment (2, 4, 9, 60, 62). A different cut-off score, less than twenty-six, was used in three studies (6, 8, 63). In one study, using the modified MMSE (1), cognitive impairment was defined by a score of less than 80/100, and cognitive decline "as an average decrease in Modified Mini-Mental State Examination score of more than 1 point per year". The cut-off scores for cognitive decline and cognitive impairment were not mentioned in nine studies (3, 5, 7, 61, 67-70, 72).
4.3. Neuroimaging
MRI or CT brain scanning were reported in six studies (1, 2, 6, 8, 9, 60, 65, 67, 68), assessing mainly for signs of ischemic stroke. Ten studies (3-5, 7, 61-63, 70-72) did not report on brain imaging.
4.4. Methodology for intima media measurement
There were a variety of methodological heterogeneity across the studies regarding IMT measurement for selected carotid artery segments (CCA, CA bulb, ICA) and carotid artery wall (near versus far) (Table 3). For IMT measurement, the CCA was used in the majority of studies (1, 2, 4-8, 60, 63, 65, 68-72). The IMT of the CA bulb was measured in one study (62), and three different locations (CCA, CA bulb, ICA) were evaluated in four other studies (3, 9, 61, 67). IMT was measured most frequently at the far wall of the CCA (2, 4, 5, 60, 63, 68, 69, 71). The far wall IMT of the CA bulb was measured in one study (62). IMT was evaluated at the far and near walls of the CCA in four studies (1, 8, 65, 72). The IMT of the near and far walls of three carotid artery segments (CCA, CA bulb, ICA) were measured in four studies (3, 9, 61, 72).
4.5. IMT and cognitive impairment
Although the methodology and study design of the 20 reported studies differed significantly, certain patterns could be noted. These patterns became more evident by differentiating the studies in post-stroke cohorts and cohorts free of vascular events.
4.5.1. Series of patients with stroke
4.5.1.1. Positive association between intima media thickness and cognitive impairment
In a longitudinal study with a one year follow-up period, Talelli et al. (2) found that IMT was significantly associated
with cognitive impairment at one-year defined by a MMSE score < 24 and after multivariate analysis. One further study (9) found that IMT was univariately associated with a six-month change in the MMSE in the control-group (45 participants), but not in the case-group (110 participants).
4.5.2. Series of patients without stroke
4.5.2.1. Positive association between intima media thickness and cognitive impairment
After a five years follow-up Johnston et al. (1) reported that increased IMT on left and right CCA were associated with increased risk of cognitive decline in univariate analysis. After adjusting for controlateral stenosis, demographics and traditional vascular risk factors, the associations were attenuated and remained significant only for the left CCA (borderline association). The Atherosclerosis Risk in Communities (ARIC) study (61) found a cross-sectional association between carotid IMT with 2 out of 3 cognitive function scales. Carotid IMT (C-IMT) was inversely associated with the Delayed World Recall Score in men and inversely correlated with the Digit Symbol Score in both genders. In a further cross-sectional study, Romero et al. (67) showed that higher internal carotid artery IMT was associated with poorer performance on the executive function factor and the nonverbal memory factor. The authors reported that the association became significant for the verbal memory factor, remained significant for the nonverbal memory factor, and was borderline for the executive function factor, after full multivariable adjustment. However, the authors noted that common carotid artery IMT was not associated with any of the cognitive measures. Cohen et al. (68) described in their cross-sectional study that increased IMT was strongly related to reduced attention, executive function, and information-processing speed. In a further cross-sectional study, Muller et al. (63) found an increased IMT to be associated with lower memory performance using the Rey auditory verbal learning test and the Doors test to assess for verbal episodic and visual memory. Haley et al. (5) underlined that a C-IMT cut-off of ≥ 0.9 mm might be relevant before higher IMT consistently relates to risk of cognitive impairment. The authors found in their cross-sectional study that an increased IMT was associated with lower attention-executive-psychomotor functioning in non-demented patients, while it was not significantly related to language, memory, or visual-spatial abilities. Komulainen et al. (62) described in their small prospective study of 91 elderly women that carotid IMT was associated with poor memory in cross-sectional and longitudinal analysis, and with cognitive speed only in the longitudinal analysis, but not with global cognitive function (assessed by the MMSE).
4.5.2.2. Negative association between IMT and cognitive impairment
In a cross-sectional study, Johnston et al. (1) reported that high IMT on the left or right CCA were associated with an increased risk of cognitive impairment in univariate analysis. However after adjustment for contralateral stenosis, demographics, and traditional vascular risk factors, these associations were modified and were no longer statistically significant. The ARIC study (3) found that IMT was longitudinally not associated with cognitive function test impairment in subjects aged 45-69 years. No association between IMT and cognitive decline after adjusting for confounding factors could be found in the cross-sectional study of Auperin et al. (4).
5. DISCUSSION
The burden of cognitive impairment and Alzheimer's disease in industrialized countries will become a major public health and economic issue. The reported rate of conversion of cognitive impairment to Alzheimer's disease is 1 to 25% per year (18). Thus, early detection of cognitive impairment will become a major concern, particularly when pharmacological intervention for preventing or delaying conversion will prove effective (14, 23). Cerebral vessel atherosclerosis is assumed to be associated with cognitive impairment through the consequences of chronic brain hypoperfusion (73, 74). Therefore, if simple IMT measurements were to predict cognitive impairment, IMT could become one of its detection tools, particularly because it is inexpensive, reliable and non-invasive. This systematic review identified twenty studies that evaluated the association between IMT and cognitive impairment and fourteen (1, 2, 5, 6, 9, 62, 63, 65, 67, 68-72) were significant after multivariate analysis. This lack of a strong relationship may in part be related to the variability in defining cognitive impairment and the heterogeneity in IMT measurement methodologies. The prime difficulty consists in defining mild cognitive impairment (MCI), differentiating normal aging from mild cognitive impairment, and differentiating mild cognitive impairment from mild dementia (15, 18, 20, 21, 44, 46). MCI, a term that appeared for the first time in the literature in 1990 (43), is not considered an established diagnosis with a single set of criteria, but rather a heterogeneous condition, for which several criteria, in recent years, were suggested (16, 17, 19, 21, 22, 44, 45). Currently MCI is a diagnosis of exclusion for patients not fulfilling the criteria of Alzheimer's disease (AD) or dementia, but who exhibit some form of cognitive impairment (specifically with memory loss, "amnestic" MCI) (18, 21, 44).
There is also a lack of consensus regarding definition and standardized measures to assess MCI (25, 26, 28, 44, 45) as well as scarce knowledge of the degree of agreement between the commonly used tests in assessing for cognition (MMSE, DSM-4, ICD-10, MDRS) (24, 27, 29). The most frequently used test in this review was the Mini Mental Status Examination (MMSE). The MMSE is considered a valuable screening instrument for the initial, formal assessment of cognition (30, 31). However, it is a tool that lacks the necessary detail for the differentiation between mild cognitive impairment and early onset dementia, especially in well educated subjects (30, 31). Furthermore, patients with visual, hearing and communication impairment(s) can not be evaluated objectively, as the MMSE is largely based on reading, writing and verbal response skills (75-77).
Consequently, in the twenty studies included in this review, a comparison of the reported results is made difficult because of the use of different cognitive tests, each evaluating a different cognitive domain. This in part could explain the divergent association with IMT. MCI is assumed to be of degenerative origin (33-36). Ten of the twenty studies (1, 3, 4, 7, 8-9, 61-63, 71) included in this review did not report on the aetiology of the observed cognitive impairment. For example, stroke or other aetiologies could have been a confounding factor in the association between cognitive impairment and IMT. Although hippocampal atrophy appears to be associated with MCI (32, 34-36), the routine role of neuroimaging in diagnosing MCI is not established as of yet (37, 49). Structural volumetric magnetic resonance imaging (MRI), single photon emission tomography (SPECT), positron emission tomography (PET) are at present the neuroimaging modalities most commonly used in patients with MCI (37, 49). The majority of the papers in this review (1, 3, 4, 7-9, 61-63, 71, 72) did not report on focused neuroimaging studies to detect specific brain alterations to sustain their diagnosis of mild cognitive impairment.
There was a huge variability in methods of IMT measurement, with regard to location, referenced IMT values and measurement techniques. This heterogeneity made it difficult to directly compare IMT results in these twenty studies. Another important methodological issue in the reviewed studies was the lack of control groups (1-5, 8, 61-63, 65, 67-71). The question of test-retest effect remains unanswered. A further limiting factor were the modest sample sizes in several studies (2, 5-7, 9, 61-63, 65, 68, 72) which consequently reduced study power and limited the generalizability of the findings. Currently, no definitive evidence of an association between increased IMT and cognitive impairment can therefore be made. Differences in age, inclusion criteria, study design, and length of follow-up may have accounted for the conflicting results. However, the present results from the investigation into the relationship between IMT and cognitive impairment remain promising. Fourteen out of the twenty reviewed studies showed a significant association after multivariate analysis (1, 2, 5, 6, 9, 62, 63, 65, 67, 68-72). Future research must establish whether increases in IMT, especially at early stages, does in fact exclusively represent atherosclerosis (10, 12, 38-40, 50, 52, 64, 78). There is also an imperative need for a consensus regarding the precise definition of cognitive impairment and the use of standardized methods in the assessment of early cognitive impairment (25), alongside a uniform way to perform IMT measurements (78) for future epidemiological studies on the relationship between IMT and cognitive impairment.
6. ACKNOWLEDGMENT
Gratefulness is expressed to Dr. Adelyn Tsu who very kindly reviewed the manuscript for the English language.
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Key Words: Carotid Intima Media Thickness, Carotid atherosclerosis, Neuropsychological test, Cognitive Impairment, Alzheimer
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