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DOI: 10.1148/radiol.2402050805
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(Radiology 2006;240:515-521.)
© RSNA, 2006

Neuroradiology

Arterial Blood Flow to the Brain in Patients with Vascular Disease: The SMART Study1

A. Fleur van Raamt, MD, PhD, Auke P. A. Appelman, MD, Willem P. T. M. Mali, MD, PhD, Yolanda van der Graaf, MD, PhD, For the SMART Study Group2

1 From the Julius Center for Health Sciences and Primary Care (A.F.v.R., Y.v.d.G.) and Department of Radiology (A.P.A.A., W.P.T.M.M.), University Medical Center Utrecht, Heidelberglaan 100, H.P. Strat. 6.131, 3584 CX Utrecht, the Netherlands. Received May 11, 2005; revision requested July 8; revision received August 8; final version accepted October 13. Supported by a program grant from the Netherlands Organization for Scientific Research-Medical Sciences (NWO-MW: project no. 904-65-095). The funding source had no involvement in the writing of this article or in the decision to submit it for publication. Address correspondence to Y.v.d.G. (e-mail: y.vandergraaf{at}umcutrecht.nl).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To retrospectively investigate which characteristics are related to total arterial blood flow to the brain in patients with symptomatic vascular disease.

Materials and Methods: The study was approved by the ethics committee of the authors' institution, and written informed consent was obtained. The total volume flow rate (tVFR) values in the internal carotid arteries and the basilar artery in 636 patients (536 men, 100 women; mean age, 58 years) with symptomatic vascular disease were measured with two-dimensional phase-contrast magnetic resonance (MR) angiography. Reference tVFR values in the general population were obtained from previous research involving 158 subjects (73 men, 85 women; mean age, 60 years).

Results: A higher tVFR was found in patients with symptomatic vascular disease, but this association was statistically significant in only those patients in the 7th decade of life. The mean tVFR decreased with increasing age (–3.4 mL/min per year; 95% confidence interval [CI]: –4.3, –2.5). Diabetes (–27.6 mL/min; 95% CI: –52.6, –2.6) and increasing body mass index (BMI) (–2.8 mL/min per BMI unit; 95% CI: –5.3, –0.2) were associated with lower tVFR. Patients with vascular disease in a cerebral location had lower tVFR values (–39.7 mL/min; 95% CI: –65.1, –14.3) than did patients with symptomatic vascular disease elsewhere in the vascular tree.

Conclusion: Patients with symptomatic vascular disease had slightly higher arterial blood flow to the brain compared with the general population. The tVFR decreased with increasing age and increasing BMI, and patients with diabetes had lower tVFR values than did those without diabetes. Patients with vascular disease in a cerebral location had lower tVFR values than did those with symptomatic vascular disease at other arterial sites.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
The vascularization of the brain can be assessed at different levels. First, the blood supply through the large vessels can be measured with two-dimensional phase-contrast magnetic resonance (MR) angiography. With this simple noninvasive technique, the volume flow rate (expressed in milliliters per minute) can be measured in both the internal carotid arteries and the basilar artery. The volume flow rates measured in these vessels are then summed to calculate the total rate of volume flow (ie, total volume flow rate [tVFR], in milliliters per minute) to the brain. By dividing this value throughout the entire brain volume, the mean cerebral perfusion can be calculated.

Second, at the brain tissue level, perfusion can be measured with different techniques such as positron emission tomography or perfusion MR imaging. These techniques can yield perfusion values in specific regions of the brain—that is, regional cerebral blood flow (rCBF) values (in milliliters per 100 g of brain tissue per minute). The cerebral blood flow in the entire brain should be similar to the tVFR corrected for the brain volume. Compared with the rCBF, the tVFR is simple and inexpensive to measure and can be easily measured in hundreds of patients. rCBF studies typically involve small sample sizes and thus have limited value in showing relationships between risk factors and flow. To show these relationships, large patient groups are required. Up to now, these smaller rCBF studies have been the only investigations available for comparison with the few tVFR studies.

A decrease in rCBF is associated with deterioration of cognitive function (1) and depression (2), and it may indicate an increased risk of cerebral ischemia (3). Several study investigators have studied the factors that influence rCBF. Contradicting results regarding the relationships between rCBF and the following variables have been described: older age (4–9), male sex (6,9), smoking (6,10–12), high amounts of alcohol intake (6,13), hypertension (6–8,14–16), hyperlipidemia (17,18), and diabetes (19). Little is known about the arterial blood flow to the brain in patients with vascular disease and the association between this flow and vascular disease risk factors. Thus, the purpose of our study was to retrospectively investigate which characteristics are related to total arterial blood flow to the brain in patients with symptomatic vascular disease.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Patients
All patients were participants in the Second Manifestations of Arterial Disease (SMART) Study, an ongoing single-center (University Medical Center Utrecht) prospective cohort study that began in September 1996. All eligible patients aged 18–79 years who were newly referred to our institution with symptomatic atherosclerosis or risk factors for atherosclerosis were screened for additional risk factors and severity of atherosclerosis. Definitions of the diseases that qualified patients for enrollment of their data in the study are reported elsewhere (20). The data for a total of 636 patients (536 men, 100 women; mean age, 58 years ± 10 [standard deviation]) were included in the study. Baseline characteristics of the patients are given in Table 1.


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  		Table 1. Baseline Characteristics of 636 Patients

 
In May 2001, MR angiography, including two-dimensional phase-contrast MR angiography, of the brain was added to the screening program for the enrolled patients with symptomatic vascular disease and without contradictions to MR angiography (ie, pacemakers, claustrophobia, and/or pregnancy). The SMART Study was approved by the ethics committee of our institution, and written informed consent was obtained from all participants. The approval and consent included those for future retrospective analyses.

For the current study, the data of 636 patients with cardiovascular disease, cerebrovascular disease, peripheral arterial disease, or abdominal aortic aneurysm for whom the results of MR angiography of the brain were available were included. Cardiovascular disease was defined as myocardial infarction or having undergone coronary surgery or percutaneous transluminal coronary angioplasty in the past or at the time of inclusion in the study. Patients with stroke or transient ischemic attack at inclusion and patients who reported having a stroke in the past were considered to have cerebrovascular disease. Peripheral arterial disease was defined as intermittent claudication or rest pain at inclusion or history of vascular surgery or angioplasty. The presence of abdominal aortic aneurysm or a history of previous surgery for it was the criterion for abdominal aortic aneurysm.

Patients with vascular disease at more than one location were assigned to more than one disease category. Patients who had internal carotid artery stenosis of 50% or greater or occlusion were excluded from the analyses. For comparison of the tVFR between the symptomatic group and the reference group, patients younger than 40 years were excluded because of their limited number (n = 21). For the other analyses, they were included.

Vascular Disease Risk Factors
At study enrollment, the subjects' risk factors were assessed by means of an extensive questionnaire and physical, ultrasonographic (US), and laboratory examinations. The subjects' height and weight were measured, and the body mass index (BMI, in kilograms per square meter) was calculated by dividing the weight by the height squared. Systolic and diastolic blood pressures (in millimeters of mercury) were measured twice with a sphygmomanometer. Hypertension was considered to be present when the mean systolic blood pressure was 160 mm Hg or higher and/or the mean diastolic blood pressure was 95 mm Hg or higher at study inclusion and/or antihypertensive treatment was being administered. A fasting venous blood sample was taken to determine glucose, lipid, and homocysteine levels. Diabetes mellitus was defined as a glucose level of 7.0 mmol/L or higher or the reported treatment for diabetes. Hyperlipidemia was defined as a total cholesterol level higher than 5.0 mmol/L, a low-density lipoprotein cholesterol level higher than 3.2 mmol/L, or the reported treatment for elevated cholesterol. Hyperhomocysteinemia was defined as a total homocysteine level of 16.3 µmol/L or higher in women or 18.8 µmol/L or higher in men.

The degree of extracranial stenosis of the internal carotid artery was assessed by using duplex US, in which the peak systolic velocity is translated into a degree of diameter reduction (21). US was also performed to measure the intima-media thicknesses (in millimeters) in the left and right common carotid arteries, as represented by the mean value of six measurements. Smoking and alcohol consumption histories were divided into three categories: never, past, and current. Patients who had quit smoking or drinking during the past year were assigned to the current category.

Sample of the General Population
Reference tVFR values were obtained from a study involving 250 adults (122 men, 128 women; age range, 19–88 years; mean age, 50 years) who had been examined with MR imaging of the brain by our research group (22). Data on the 158 individuals (73 [46%] men; mean age, 60 years) who were aged 40–79 years among these 250 subjects were used for the current analysis. This population consisted of 79 individuals who were first-degree relatives of patients with subarachnoid hemorrhage and had been screened for the presence of intracranial aneurysms and 79 elderly persons who were participating in a population-based study. The tVFR values in this group had been measured with ungated two-dimensional phase-contrast MR angiography by using the same technique used to examine the patient group in our current study.

MR Angiography
The MR examinations were performed by using a 1.5-T whole-body system (Gyroscan ACS-NT; Philips Medical Systems, Best, the Netherlands). On the basis of findings on a localizer MR angiographic slab in the sagittal plane, a two-dimensional phase-contrast section was positioned at the level of the skull base to measure the volume flow in the internal carotid arteries and the basilar artery. The Figure illustrates the positioning of the two-dimensional phase-contrast section (16/9 [repetition time msec/echo time msec]; flip angle, 7.5°; section thickness, 5 mm; field of view, 250 x 250 mm; matrix size, 256 x 256; eight acquired signals; velocity sensitivity, 100 cm/sec) through the internal carotid arteries and the basilar artery. Postprocessing was performed by specialized MR technologists with more than 5 years of experience. Two images obtained with opposed, bipolar, velocity-encoding gradients were subtracted to achieve velocity sensitivity.


Figure 1
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  		Left: Sagittal localizer MR angiogram illustrates the positioning of a two-dimensional phase-contrast MR angiographic section (16/9, 7.5° flip angle) for measurement of the volume flow through the internal carotid arteries and the basilar artery. Right: Quantitative flow values were obtained by means of integration across manually drawn regions of interest (on corresponding two-dimensional phase-contrast MR angiographic image) that enclosed the vessels. 1 = right-sided internal carotid artery, 2 = left-sided internal carotid artery, 3 = basilar artery. Line through the left image indicates the plane of the right image.

 
For each vessel, the spatial and time-averaged flow velocity was calculated from the phase-difference images by manually drawing a region of interest around the vessel. Special care was taken to ensure that the region of interest encompassed the entire lumen of the vessel without including too many stationary tissue voxels (Figure). The surrounding stationary tissue voxels included in the region of interest were not expected to affect accuracy, since such voxels do not carry flow. The flow velocity in each vessel was multiplied by the cross-sectional area of the pixels in the region of interest to obtain the volume flow rate. Good agreement between repeated volume flow rate measurement postprocessing procedures was revealed for hand-drawn regions of interest in our research group, with a coefficient of variation of 5% (23). The flow through the left and right internal carotid arteries and the basilar artery was summed to calculate the tVFR (in milliliters per minute).

Statistical Analyses
The ages of the symptomatic patients were categorized by decade, as was done for the sample of the general population (22). In each age group, the mean tVFR ± the standard deviation was calculated for the male and female subjects separately and for the group as a whole. Since the raw data of the sample of the general population were no longer available, differences in tVFR between populations and differences between the sexes were determined with an unpaired Student t test (CIA 1.0; BMJ Publishing, London, England) to result in a tVFR difference. A 99% confidence interval (CI) was calculated to adjust for multiple comparisons.

We assessed the effects of age, other risk factors, and vascular disease location on the tVFR by using linear regression analysis (SPSS 12.0.1; SPSS, Chicago, Ill) after checking whether the continuous variables were normally distributed. For each factor, we calculated the crude and age-adjusted regression coefficients, ß, which yield the slope of the regression fitted by the model and indicate the increase (positive value) or decrease (negative value) in tVFR, in milliliters per minute per unit of the independent variable. The crude regression coefficient was determined for all risk factors and vascular disease locations. We calculated an age-adjusted regression coefficient by including subject age in the model. For all test results, 95% CIs, being more informative than P values, were given (24). A 95% CI that did not include the value of 0 had a P value of less than .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
The tVFR was higher in the patients with symptomatic vascular disease than in the reference group, among all age groups. However, the difference was significant in only those patients in the 7th decade of life; the difference in tVFR was 55 mL/min (95% CI: 12, 98) (Table 2). A decrease in tVFR with increasing age was observed. No significant differences in tVFR between the male and female subjects were observed.


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  		Table 2. Age-based MR Angiographic tVFR Measurements in Patients with Symptomatic Vascular Disease and Healthy Subjects

 
All continuous variables in the patient group were normally distributed. tVFR decreased with increasing age (Table 3). When we analyzed each risk factor separately with adjustments for age, diabetes (–27.6 mL/min; 95% CI: –52.6, –2.6) and BMI (–2.8 mL/min per BMI unit; 95% CI: –5.3, –0.2) were associated with a decrease in tVFR. Patients with cerebrovascular disease clearly had lower tVFR values than did those without it; this difference remained when age was taken into account (–39.7 mL/min; 95% CI: –65.1, –14.3).


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  		Table 3. Crude and Age-adjusted Regression Coefficients for Individual Risk Factors and Location of Vascular Disease, with tVFR as Dependent Variable

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 References
 
Our study results show that the patients with vascular disease had a slightly higher tVFR overall than did the sample of the general population. In the patient group, the tVFR decreased with increasing age and increasing BMI and was lower in the patients with diabetes. Furthermore, the patients with vascular disease in a cerebral location had lower tVFR values than did the patients with vascular disease in other locations.

To date, we are unable to predict which patients with risk factors for vascular disease will have symptomatic cerebrovascular disease. In our opinion, the population that should be targeted for research of cerebral blood flow is that of high-risk patients who have at least one manifestation of vascular disease. To prevent the presence of internal carotid artery stenosis from confounding the results, we restricted our study to patients who had neither 50% or greater stenosis nor occlusion at baseline.

We chose a reference group that was not entirely free of vascular disease but represented a sample of the general population. If the results were influenced by this decision, the difference in tVFR could have been only underestimated. In the reference group, the same two-dimensional phase-contrast MR imaging technique was used to measure the tVFR. In a study to compare methods of measuring blood flow volume, flow values differed widely among different techniques (25), implying the need to use the same method for every consecutive or comparative flow measurement.

A comparison of the results obtained by different investigators revealed a wide range of tVFR values, which were in good agreement with the internal carotid artery values but slightly lower than the basilar artery values in our reference group (22). In our opinion, since the methods used to measure the tVFR in our patient group and the reference group were exactly the same and the patient numbers were relatively high compared with those in many other studies, it was unlikely that the difference in flow between the two groups was based on chance.

Volume flow rate measurement in patients with vascular disease or in healthy control subjects is described in few small-sample studies (26–29). The main focus in the literature is measurement of rCBF in patients with cerebrovascular disease rather than measurement of the total arterial flow to the brain.

We expected the patients with vascular disease to have a lower tVFR than the sample from the general population. In contrast, the tVFR was slightly higher in the patients with vascular disease. An explanation could be that the inflammatory process related to atherosclerosis results in elevated tVFR values. We have found no other studies in which greater flow in a similar patient group was reported.

In our study, the tVFR decreased 34 mL/min per decade. Investigators in a longitudinal study reported that rCBF decreases with increasing age and with progressive cerebrovascular disease (6). The relationship between lower rCBF and increasing age has been reported in cross-sectional studies with healthy volunteers (5,8,9,22), while another study revealed that the main relationship was increasing atherosclerosis with increasing age (4) and another study revealed no relationship between age and rCBF (7).

The longer duration of diabetes was reported to be related to lower rCBF in a patient group with insulin-dependent diabetes (30). Investigators in another study proposed that the relationship between diabetes and rCBF may accelerate the age-related reduction in rCBF (19). Diabetes is also related to cerebral atrophy (31). The arterial occlusive disease associated with diabetes, together with the lower brain volume due to atrophy, might explain the lower tVFR values in the patients with diabetes observed in our study. The observed lower flow in patients with increasing BMI could have been due to the high prevalence of diabetes in patients with a high BMI.

Our study results also show that cerebrovascular disease is related to lower tVFR. Since this was a cross-sectional study, it is impossible to say which came first: the cerebrovascular disease or the lower tVFR. However, because the relationship between increasing age and lower tVFR is well established and because in our study diabetes also was related to lower tVFR, it seems more probable that the lower tVFR was an effect of the progression of disease. Internal carotid artery stenosis cannot be an explanation for this relationship because patients with stenosis of 50% or greater were excluded from this study. Since generalized atherosclerotic disease cannot account for the observed relationship, we speculate that more distally located obstructive disease in the cerebral vessels or the smaller brain volume necessitating blood after a stroke could have accounted for the correlation.

A limitation of our study was the absence of data on brain volume. For comparison of the rCBF data with our arterial flow data in particular, brain volume data were needed. The purpose of our study was not to compare our data with those obtained with other modes of measuring cerebral blood flow but rather to evaluate the determinants of the total rate of volume flow to the brain. It is known that the average weight of the cerebrum decreases with age (32). We believe that in our analyses, after adjustments for age, our results were not confounded by brain volume differences. Differences in brain volume due to disease—for example, diabetes—could very well be an explanation for the observed results. However, this remains an assumption.

Another limitation was that all patients with transit ischemic attack or stroke at inclusion were considered to have cerebrovascular disease. Cardiovascular disease could have been the real cause of the transit ischemic attack or stroke. We did not have enough information to make this distinction. If the results were affected by this possible misclassification, then it could have caused some underestimation.

The patients included in our study were newly referred to our university hospital with a clinical manifestation of cerebral, cardiac, or peripheral vascular disease, or an abdominal aortic aneurysm. In our opinion, no selection bias occurred at study inclusion. However, the generalizability of our study findings could be confined to academic hospitals since patients with more severe disease are expected to visit these facilities.

Our study results show that patients with vascular disease have slightly higher tVFR values than do healthy subjects; that age, BMI, and diabetes are related to tVFR; and that patients with vascular disease in a cerebral location have lower tVFR values than do patients with symptomatic vascular disease elsewhere in the vascular tree. The cause of the lower tVFR values in the patients with cerebrovascular disease will have to be unraveled in future research, because the process of generalized atherosclerosis alone apparently cannot explain our results.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
References
 


   ACKNOWLEDGMENTS
 
We gratefully acknowledge the members of the SMART Study Group of University Medical Center Utrecht: A. Algra, MD, FAHA, Julius Center for Health Sciences and Primary Care and Rudolf Magnus Institute for Neurosciences, Department of Neurology; J. D. Banga, MD, PhD, and F. L. J. Visseren, MD, PhD, Department of Vascular Medicine; P. A. Doevendans, MD, PhD, Department of Cardiology; B. C. Eikelboom, MD, PhD, and F. L. Moll, MD, PhD, Department of Vascular Surgery; D. E. Grobbee, MD, PhD, and G. E. H. M. Rutten, MD, PhD, Julius Center for Health Sciences and Primary Care; L. J. Kappelle, MD, PhD, Department of Neurology; and H. A. Koomans, MD, PhD, Department of Nephrology.


   FOOTNOTES
 

Abbreviations: BMI = body mass index • CI = confidence interval • rCBF = regional cerebral blood flow • tVFR = total volume flow rate

2 Members of the SMART Study Group are listed in the Acknowledgments. Back

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, Y.v.d.G.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, A.F.v.R., A.P.A.A.; clinical studies, A.F.v.R., A.P.A.A.; statistical analysis, A.F.v.R., A.P.A.A., Y.v.d.G.; and manuscript editing, all authors


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 

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