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Published in final edited form as:
J Clin Exp Neuropsychol. 2012 ; 34(2): 220–225. doi:10.1080/13803395.2011.630653.
Cerebral Blood Flow and Neuropsychological Functioning in
Elderly Vascular Disease Patients
David J. Moser1,*, Laura L. Boles Ponto2, Ivy N. Miller3, Susan K. Schultz1, Yusuf Menda2,
Stephan Arndt1, and Peggy C. Nopoulos1
1Department of Psychiatry, University of Iowa Carver College of Medicine, Iowa City, IA, USA
2Division
of Nuclear Medicine, Department of Radiology, University of Iowa Carver College of
Medicine, Iowa City, IA
3Department
of Psychology, Boston University, Boston, MA, USA
Abstract
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This study was designed to determine the relationships between PET-based quantitative measures
of cerebral blood flow and cerebrovascular reserve and neuropsychological functioning in elderly
individuals with atherosclerotic vascular disease. It was hypothesized that cerebrovascular
function would be significantly associated with neuropsychological functioning. Results showed
that both baseline global cerebral blood flow and cerebrovascular reserve were significantly
associated with global neuropsychological functioning, when controlling for age and sex.
Cerebrovascular reserve was additionally associated with performance on measures of memory
and attention. Additional research is needed to determine whether measures of cerebral blood flow
can be used to predict cognitive decline.
INTRODUCTION
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There is a vast literature demonstrating the negative effects of vascular disease, and
particularly cerebrovascular disease, upon cognition. Indeed, although Alzheimer’s disease
(AD) remains the leading cause of dementia in the U.S., it has been estimated that
cerebrovascular disease is a contributing factor in over half of all cases of dementia,
regardless of dementia subtype (Breteler, 2000). The existence of common risk factors, i.e.,
hypertension, diabetes, obesity, hyperlipidemia and apolipoprotein ε4 genotype, for both
Alzheimer’s and vascular dementia (Iadecola, 2004; Naderali, Ratcliffe, & Dale, 2009) and
the positive effects of the treatment of vascular risk factors on cognitive decline in patients
with AD without cerebrovascular disease (Deschaintre, Richard, Leys, & Pasquier, 2009)
reinforce the view that in the least, the pathologies are intricately linked. Similarly,
atherosclerotic vascular disease (AVD) has been associated with cognitive dysfunction and
dementia. However, relatively few studies focus on the earliest stages of this process, prior
to the development of significant cognitive decline. Previous studies from our lab have
revealed significant relationships between forearm vascular function (a measure of overall
vascular health) and global neuropsychological performance (Moser et al., 2004; Moser et
al., 2007) as well as initiation and processing speed (Moser et al., 2008) in elderly
individuals with AVD. Given the public health significance of both dementia and vascularrelated diseases, it is important to gain a better understanding of the relationship between
cerebrovascular health and cognition, particularly among individuals who do not yet have
*
Correspondence: David J. Moser, Ph.D., Department of Psychiatry – W278 GH, University of Iowa Carver College of Medicine, 200
Hawkins Drive, Iowa City, IA 52242, david-moser@uiowa.edu, Telephone: 319-384-9211, Fax: 319-353-8656.
Note: This manuscript is not under review at any other journal. The authors do not have any conflicts to disclose.
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advanced disease (e.g. stroke, vascular dementia), as early intervention may help prevent or
at least attenuate the disease processes.
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The purpose of the present study was to examine the relationship between cerebrovascular
function as characterized by quantitative measures of cerebral blood flow (gCBF) and
cerebrovascular reserve (CVR) and neuropsychological performance in a sample of elderly
individuals with atherosclerotic vascular disease who had no history of stroke, cardiac
surgery, or dementia diagnosis. It was hypothesized that higher levels of cerebral blood flow
would be significantly and positively associated with neuropsychological performance.
METHODS
This research was approved by the University of Iowa Institutional Review Board and all
participants provided written informed consent following a thorough discussion of the study.
Participants
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Participants were 14 elderly individuals with atherosclerotic vascular disease (10 men, 4
women; Mean age = 68 years, SD = 6; Mean education = 16 years, SD = 4) who were
already enrolled in our ongoing program of research on aging, cognition and vascular
disease. All participants had an unequivocal diagnosis of AVD with a history of one or more
of the following: angina pectoris, myocardial infarction, percutaneous transluminal coronary
angioplasty, placement of coronary artery stent, and peripheral vascular disease
(claudication). All female participants were post-menopausal and none were on hormone
replacement therapy. Exclusion criteria included history of coronary artery bypass grafting,
valve replacement, carotid endarterectomy, stroke, head injury with loss of consciousness
longer than 30 minutes, other neurological disorder or systemic illness unrelated to vascular
disease that was likely to affect cognition, focal neurological sign, diagnosis of dementia,
renal disease, hepatic disease, gout, adrenocortical insufficiency, and current or past severe
psychiatric illness (e.g. bipolar affective disorder, schizophrenia). Additional exclusion
criteria included taking warfarin (due to increased risk of bleeding during placement of an
arterial line), taking any medication with known cerebrovascular activity, and known
sensitivity to carbonic anhydrase inhibitors or antibacterial sulfonamides, thiazide diuretics,
or other sulfonamide-derivative diuretics. Participants were asked to refrain from consuming
alcohol for 24 hours prior to the study and caffeine for three hours prior to the study.
Neuropsychological Assessment
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All participants underwent a large battery of standardized and well-established
neuropsychological tests administered by a trained research assistant under the supervision
of a licensed psychologist (D.J.M.). For the purposes of the current study, the Repeatable
Battery for the Assessment of Neuropsychological Status (RBANS) was used to assess level
of neuropsychological functioning (Randolph, 1998). This widely-used battery consists of
12 subtests and yields a Total Scale Score that indicates level of global neuropsychological
functioning, in addition to five Index Scores including Immediate Memory, Delayed
Memory, Attention, Language and Visuospatial/Constructional.
Assessment of Cerebral Blood Flow and Cerebrovascular Reserve
Participants underwent quantitative [15O]water PET imaging with arterial blood sampling
for the determination of global cerebral blood flow (gCBF: mL/min/100mL of tissue) during
a simple counting task and during a list recall task. Additionally, gCBF was measured a third
time as participants completed the counting task following the administration of the carbonic
anhydrase inhibitor acetazolamide (ACZ), in order to assess cerebrovascular reserve, the
ability of the brain to increase blood flow when induced to do so. Technical methodology
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was implemented as previously described for work at this institution (Boles Ponto, Schultz,
Watkins, & Hichwa, 2004; Hichwa, Ponto, & Watkins, 1995; Hurtig et al., 1994; Ponto,
Magnotta, Moser, Duff, & Schultz, 2006). Imaging was performed on a Siemens ECAT
EXACT HR+ scanner.
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Three [15O]water injections (50 mCi per injection) for the measurement of gCBF were
performed, two at baseline (i.e., non-vasodilated state) and a third 15 minutes after the
intravenous administration of a 1 g bolus of ACZ (Kuwabara, Ichiya, Sasaki, Yoshida, &
Masuda, 1995). At baseline, imaging was performed during a simple counting task and
during a list recall task, whereas, in the vasodilated state, only the counting task was utilized.
The counting task required participants to count “1-2-3, 1-2-3” at an approximate rate of one
number per second. In preparation for the memory task, participants were read the Rey
Auditory Verbal Learning Test (Rey, 1964) 15-item word list five times. After each
presentation of the list, participants were asked to recall aloud as many of the list words as
possible. Approximately one hour later, while in the scanner, participants were asked to
recall as many of the list words as possible and to continuously recall the list even if it meant
having to repeat words they had already stated, until instructed to stop. Participants were
instructed to begin the counting or memory task 10 seconds prior to the arrival of the bolus
of [15O]water in the brain, and to continue as described for the specified task for the 100
seconds of image acquisition. Arterial blood sampling, using an on-line sampler
(Wollenweber, Hichwa, & Ponto, 1997) began simultaneously with the injection of the
[15O]water. Activity images were created by summing the forty seconds post-bolus transit
and iteratively reconstructing the summed data (2 iterations/8 subsets, zoom = 2.57,
Gaussian filter = 5.0 mm). Parametric images were calculated from the activity images and
the arterial blood curve using the pixel-wise modeling module of the PMOD software
package (PMOD Technologies, Ltd, Zurich, Switzerland, http://www.pmod.com/
technologies/index.html). Global cerebral blood flow for each of the conditions (baseline
counting task, during list recall, after administration of acetazolamide) was determined by
averaging all intracerebral pixels excluding ventricular spaces.
Statistical Analysis
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Throughout the statistical analysis, gCBF during the simple counting task was used as the
measure of “baseline” gCBF. The relationships of baseline gCBF and gCBF during the list
recall task to global neuropsychological functioning (RBANS Total Scale Score) were
examined using partial correlations, controlling for age and sex. An additional partial
correlation was calculated between gCBF during the list recall task and RBANS Total Scale
Score while controlling for age, sex, and baseline gCBF. The relationship between CVR and
global neuropsychological functioning was examined by calculating the partial correlation
between gCBF after administration of acetazolamide and RBANS Total Scale Score,
controlling for age, sex, and baseline gCBF. Finally, follow-up partial correlations
(controlling for the same variables as above) were calculated between measures of gCBF,
CVR, and more specific measures of neuropsychological functioning (the five RBANS
Index Scores).
RESULTS
Descriptive statistics for disease-related variables, PET and neuropsychological variables are
presented in Tables 1 and 2. As a group, participants performed in the average range with
regard to global neuropsychological function (RBANS Total Scale Score) and on all five
RBANS Index scores. There was no statistically significant difference observed between
measures of gCBF taken during the baseline counting task and the list recall task [t (13) = −.
59, p = .567]. As expected, there was a significant increase in gCBF after administration of
ACZ as compared to during the baseline counting task [t (13) = −8.50, p < .001].
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Table 3 shows the relationships among baseline gCBF, gCBF during list recall, CVR, and
cognition. Specifically, when controlling for age and sex, there were significant and positive
relationship between baseline gCBF and RBANS Total Scale Score [partial r = .581 (df =
10), p = .047], and between gCBF during list recall and RBANS Total Scale Score [partial r
= .623 (df = 10, p = .031]. However, it should be reiterated here that gCBF did not
significantly increase above baseline during the list recall task. Furthermore, the relationship
between gCBF during list recall and RBANS Total Scale Score was rendered nonsignificant
when controlling for baseline gCBF [partial r = .467 (df = 9), p = .148]. This is discussed
later in the manuscript.
With regard to cerebrovascular reserve, it was found that when controlling for age, sex, and
baseline gCBF (i.e. while counting), there was a significant relationship between gCBF after
administration of ACZ and RBANS Total Scale Score [partial r = .604 (df = 9), p = .049].
Follow-up analyses revealed significant relationships between CVR and two more specific
aspects of cognition (RBANS Delayed Memory, Attention Index Scores).
DISCUSSION
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In this study of elderly individuals with atherosclerotic vascular disease, baseline gCBF,
gCBF during list recall, and CVR (cerebrovascular reactivity to acetazolamide) were all
significantly and positively associated with pre-scan performance on a measure of global
neuropsychological function. CVR was also significantly associated with performance on
more specific pre-scan measures of memory and attention. The measure of gCBF during list
recall was not significantly associated with global neuropsychological function when
controlling for baseline gCBF.
Although there are very few published studies that have examined the relationship between
quantitative gCBF measures and cognition, our findings of significant relationships between
gCBF, CVR and neuropsychological status are consistent with expectations based on brain
physiology. It is commonly accepted that while the brain accounts for only approximately
3% of body weight, it consumes 20% or more of available oxygen and glucose.
Consequently, disrupted perfusion, whether severe and acute or subtle and chronic, would
naturally be expected to affect brain function.
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It is intriguing, however, that the above relationships between measures of cerebrovascular
health and neuropsychological status were evident in this sample of individuals who had
atherosclerotic vascular disease, but no history of stroke, cardiac surgery, or dementia
diagnosis. These participants, therefore, may have experienced only very mild, if any,
vascular cognitive decline. Indeed, as a group, they performed in the average range with
regard to global neuropsychological function (RBANS Total Scale Score) and across all five
RBANS Index scores. The fact that the above relationships were found speaks not only to
the significant association between relatively early-stage vascular disease and
neuropsychological status, but also the sensitivity of the methodology employed in this
study. We would expect that the relationships between measures of gCBF and cognition
would be even stronger in a sample with a greater range of vascular disease severity and
cognitive dysfunction.
In a recent study, Kitagawa and co-investigators (Kitagawa et al., 2009) found that, among
27 cognitively intact individuals with hypertension and white matter abnormalities on brain
MRI, those showing cognitive decline across a three-year period had significantly lower
baseline gCBF values than those who did not show such decline (Mean = 31.2, SD = 2.4 vs.
Mean = 42.6, SD = 5.9 mL/min/100g). Interestingly, however, there was not a significant
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relationship between gCBF and cognitive status at baseline. Additionally, baseline CVR was
found not to be significantly related to cognition at baseline or follow-up.
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There are some key differences between the Kitagawa study and the current one. Although
both studies found relationships between cognition and gCBF, Kitagawa observed this
relationship with cognitive decline across time rather than with baseline cognitive function.
These differences could be due to the measures used to assess cognitive function and/or
statistical analysis. It is important to note that the Kitagawa study used only the MMSE to
assess cognitive function, a very basic assessment tool, whereas, the current investigation
utilized the RBANS, an instrument which provides a more comprehensive assessment of
neuropsychological status. Specifically, the RBANS assesses memory and attention more
thoroughly than does the MMSE, and the RBANS includes a measure of psychomotor
processing speed (the Coding subtest, which is incorporated into the Attention Index Score),
while the MMSE has no such measure. Given that psychomotor slowing is well known to be
associated with cerebrovascular disease (Roman, 2005) it is essential to assess this aspect of
cognitive function in studies on the relationship between vascular disease and
neuropsychological performance. Furthermore, data analysis in the current study included
controlling for age and sex, while neither of these factors was taken into account in the
Kitagawa study. In that study, the group of participants who experienced cognitive decline
across time consisted entirely of men, while the group that did not experience cognitive
decline consisted of only 43% men, underscoring the potential importance of taking sex into
account when studying the relationship between vascular disease and cognition. Regardless
of the specific differences between the studies, it should be reiterated that both studies found
significant relationships between gCBF and cognition in non-demented individuals with
vascular disease.
As noted above, the significant relationship observed between gCBF during the list recall
task and global neuropsychological function failed to reach statistical significance when
controlling for baseline gCBF. It is important to reiterate that gCBF did not increase
significantly above baseline during the list recall task. Therefore, the significant relationship
that was observed between gCBF during the list recall task and global neuropsychological
functioning serves primarily as a within-study replication of the finding that baseline gCBF
is associated with global neuropsychological functioning. It does not clarify whether degree
of gCBF increase during an in-scanner cognitive task is associated with global
neuropsychological functioning.
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Regarding limitations of the current study, the sample consisted of relatively highlyeducated individuals and, therefore, the above results may not generalize to the larger
population of individuals with vascular disease. It is also important to note that this study
did not include a healthy elderly comparison group. Lacking this, it remains unclear whether
the observed relationships between quantitative measures of gCBF and neuropsychological
status are unique to elderly individuals with AVD or whether they also exist as part of the
continuum of “normal aging.” It should also be noted that the above correlations may give
the appearance that CVR correlates more strongly with cognitive function than does baseline
gCBF. However, given our sample size, the confidence intervals surrounding these
correlations would be expected to be fairly wide and, thus, we lack adequate power to
determine whether the correlations are of significantly different magnitude. Additionally,
given the cross-sectional nature of the study, we were unable to determine whether our
measures of gCBF are predictive of future cognitive decline as observed by Kitagawa (16).
Given the high prevalence of vascular disease, its strong association with
neuropsychological dysfunction, and downstream effects on daily functioning and quality of
life, it is essential that we gain a clearer understanding of the earliest stages of vascular
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cognitive impairment. This cross-sectional study revealed significant and positive
relationships between baseline gCBF, CVR and neuropsychological performance in a
sample of elderly individuals with atherosclerotic vascular disease, with no history of stroke,
cardiac surgery, or dementia diagnosis. Additional longitudinal research is needed to
determine the degree to which measures of gCBF and CVR can be used to identify those
individuals who are at greatest risk for future vascular-related cognitive decline and/or the
development of Alzheimer’s disease.
Acknowledgments
This study was funded by grants to Dr. David J. Moser from the National Institute on Aging (1 R03 AG024609-01)
and the American Federation for Aging Research. Additional support was provided by the University of Iowa
General Clinical Research Center (Grant RR00059 from the General Clinical Research Centers Program, National
Center for Research Resources, NIH). The authors would like to thank Christine Sinkey for assistance in
coordinating laboratory procedures.
References
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Table 1
Descriptive Statistics for Vascular Disease-Related Variables
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Variable
Mean
SD
Duration of illness (years)
10.29
6.34
Body Mass Index
29.64
5.02
Number of antihypertensive drugs
2.21
1.19
Systolic blood pressure, mm HG
128.00
22.11
Diastolic blood pressure, mm HG
69.93
9.09
Total cholesterol, mg/dl
161.79
42.47
HDL-C, mg/dl
53.50
17.24
LDL-C, mg/dl
88.08
32.21
Triglycerides, mg/dl
111.31
60.10
Glucose, mg/dl
112.29
25.71
Note. Duration of illness = years since first onset of clinically-significant vascular disease symptoms. Number of antihypertensive drugs = number
currently prescribed per participant. Participants fasted prior to blood draw. HDL-C = high-density-lipoprotein cholesterol. LDL-C = low-densitylipoprotein cholesterol.
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Table 2
Descriptive Statistics for Cerebral Blood Flow and Neuropsychological Data
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Variable
Mean
SD
percentile
gCBF during counting task (baseline gCBF)
41.4
5.2
N/A
gCBF during list recall
42.0
5.5
N/A
gCBF after administration of ACZ
59.3
11.1
N/A
RBANS Total Scale Score
102.43
9.40
55
Immediate Memory
102.14
10.40
55
Delayed Memory
101.07
10.42
53
Attention
99.57
8.64
50
Language
101.00
9.72
53
Visuospatial/Constructional
107.14
13.21
68
Note. gCBF = global cerebral blood blow; ACZ = Acetazolamide; All gCBF values are expressed as mL/min/100mL of tissue; RBANS:
Repeatable Battery for the Assessment of Neuropsychological Status; RBANS scores are age-corrected standard scores (normative Mean = 100;
SD = 15).
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Table 3
Relationships Between Cerebral Blood Flow and Neuropsychological Performance
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Baseline gCBF Partial r
gCBF during list recall Partial r
.581*
.623*
.604*
Immediate Memory
.493
.228
.459
Delayed Memory
.219
.389
.625*
Attention
.465
.805*
.738*
Language
.282
.122
−.257
Visuospatial/Constructional
.428
.516
.212
RBANS Total Scale Score
gCBF after ACZ Partial r
Note.
*
p < .05;
gCBF = global cerebral blood flow; ACZ = Acetazolamide; r values represent partial correlations. Baseline gCBF and gCBF during list recall
correlations were calculated controlling for age and sex. gCBF after administration of ACZ correlations were calculated controlling for age, sex,
and baseline gCBF.
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