Assessment of Cerebral Blood Flow by Means of
Blood-Flow-Volume Measurement in the Internal
Carotid Artery
Comparative Study With a
133
Xenon Clearance Technique
J.F. Soustiel, MD; T.C. Glenn, PhD; P. Vespa, MD; B. Rinsky; C. Hanuscin; N.A. Martin, MD
Downloaded from http://stroke.ahajournals.org/ by guest on June 16, 2017
Background and Purpose—We sought to evaluate a new, angle-independent ultrasonic device for assessment of blood
flow volume (BFV) in the internal carotid artery (ICA).
Methods—Nineteen patients and 4 healthy volunteers were enrolled in a comparative study conducted in the Care Unit of
the Division of Neurosurgery at UCLA Medical Center. All patients had been admitted because of severe brain injury:
15 patients with severe head trauma (Glasgow Coma Scale scoreⱕ8) and 4 patients with subarachnoid hemorrhage due
to aneurysm rupture. In all patients and subjects, cerebral blood flow (CBF) values obtained with the 133xenon-clearance
technique were compared with BFV measurements in the ipsilateral ICA.
Results—Hemispheric CBF values showed a close and linear correlation with BFV measurements (r⫽0.76, P⬍0.0001).
Global CBF values showed a higher correlation with the total BFV value obtained from both ICAs (r⫽0.84, P⬍0.0001).
With 37 mL · min⫺1 · 100 g⫺1 as a cutoff value for the ischemic range, a BFV value of 220 mL/min would yield a positive
predictive value of 91.7% and a negative predictive value of 82.6% (sensitivity 73.3%, specificity 95%). Conversely,
BFV sensitivity and specificity were 60% and 96%, respectively, for the hyperemic range defined by a CBF value ⬎55
mL · min⫺1 · 100 g⫺1 (positive predictive value of 85.7% and negative prediction value of 85.7%).
Conclusions—BFV measurements with this new technology proved to accurately correlate with CBF values evaluated by
the 133xenon-clearance technique. These results support the implementation of this technique for bedside assessment of
cerebral hemodynamics in critically ill neurosurgical patients. (Stroke. 2003;34:1876-1880.)
Key Words: cerebral blood flow 䡲 hemodynamics 䡲 ultrasonography, Doppler
D
uring the past 2 decades, there has been a continuous
trend of increasing efforts toward the refinement of
neuromonitoring technologies. Because most of the pathologic processes that affect the acutely injured brain might
eventually result in impairment of cerebral blood flow (CBF),
early identification of ischemia or hyperemia might be critical
to define the most appropriate therapeutic strategies. Not
surprisingly, numerous modalities have been developed and
applied to the evaluation of CBF in neurosurgical patients,
although such modalities seldom fit the reality of neurointensive care patients.1 Isotopic studies such as positron emission
tomography, single-photon emission tomography, and imaging studies such as stable xenon computed tomography and
magnetic resonance imaging– based technology have all
proved to achieve reliable and accurate measurements of
CBF. All of these techniques, however, are cumbersome and
expensive and most important, imply the transfer of critically
ill and often sedated and ventilated patients to the imaging or
radionuclear facility. As such, these techniques cannot be
repeated as clinically indicated and therefore, are of limited
use in the clinical setting of intensive care. In an attempt to
develop CBF measurement capabilities at the patient’s bedside, attention has been drawn to clearance techniques, such
as the Kety-Schmidt2 or the 133xenon-clearance3 technique.
These techniques, particularly the Kety-Schmidt technique,
have proved to be reliable and accurate, especially when
incomplete diffusion equilibrium for the inert gas tracer
between the brain and its venous blood is taken into consideration and corrected.4 Nevertheless, both methods are limited by specific technical drawbacks. The Kety-Schmidt
technique is invasive and provides a global CBF assessment
that does not take into consideration possible asymmetry in
the jugular veins. The 133xenon-clearance technique, on the
other hand, is limited by personal safety issues, such as
repeated exposure of patients to radioactive tracers, as well as
possible contamination by external carotid vessels.1
Received January 5, 2003; final revision received March 15, 2003; accepted April 8, 2003.
From the Cerebral Blood Flow Laboratory and Brain Injury Research Center (T.C.G., P.V., B.R., C.H., N.A.M.), Division of Neurosurgery, David
Geffen School of Medicine, University of California at Los Angeles, and the Department of Neurosurgery (J.F.S.), Rambam Medical Center, Technion,
B. Rappaport Faculty of Medicine, Haifa, Israel.
Correspondence to Neil A. Martin, MD, Division of Neurosurgery, David Geffen School of Medicine, University of California at Los Angeles, Los
Angeles, CA 30095. E-mail [email protected].
© 2003 American Heart Association, Inc.
Stroke is available at http://www.strokeaha.org
DOI: 10.1161/01.STR.0000080942.32331.39
1876
Soustiel et al
Eventually, the urgent need for reliable data on cerebral
hemodynamics status has led to the implementation of indirect methods of CBF approximation in the neuromonitoring
armamentarium, such as transcranial Doppler, jugular bulb
oxymetry, and near-infrared spectroscopy. Unfortunately,
none of these has reached a level of accuracy that would
allow critical therapeutic decisions to be made.
As a result, increasing attention has been drawn to the
potential value of ultrasound Doppler technology for the
measurement of blood flow volume (BFV) in the internal
carotid artery (ICA) as a correlate for hemispheric CBF. A
recent report has suggested the implementation of digital
Doppler ultrasound and angle-independent dual-beam technology for improvement of accuracy in the assessment of
hemispheric CBF.5 The aim of the present study was to
evaluate this novel ultrasound device by means of the
133
xenon-clearance technique.
Downloaded from http://stroke.ahajournals.org/ by guest on June 16, 2017
Methods
CBF Assessment by Means of BFV Measurement
1877
Figure 1. Schematic representation of the angle-independent
dual-beam Doppler ultrasound (FlowGuard) device. This technology uses 2 ultrasound beams, L1 and L2, which cross the
vessel lumen with a known angle ␣ between them, and allows
the simultaneous acquisition of hundreds of small sample volumes (small dots) of ⬍200 ␮m depth along L1 and L2. This in
turn allows the accurate determination of flow velocity profile,
vessel diameter (D), and insonation angles (␪1 and ␪2).
Patients
Nineteen patients and 4 healthy volunteers were enrolled in this
study. All were studied in the Neurointensive Care Unit of the
Division of Neurosurgery at UCLA Medical Center. Informed
consent was obtained, in compliance with guidelines of the UCLA
Medical Institutional Review Board. All patients were admitted to
UCLA Medical Center because of severe brain injury: 15 with severe
head trauma (Glasgow Coma Scale scoreⱕ8) and 4 with subarachnoid hemorrhage due to aneurysm rupture. There were 16 men and
7 women, ranging in age between 20 and 75 years (age, 38.9⫾16.1
years).
Management Protocol
After initial evaluation in the emergency department and surgery as
clinically indicated, patients were admitted to the intensive care unit.
According to their clinical condition, patients received routine
management, including ventilation and sedation as indicated. Intracranial pressure was managed by intravenous administration of
mannitol and barbiturates. Fluids and vasopressors were administered to maintain cerebral perfusion pressure above the ischemic
threshold. Routine monitoring included intracranial pressure, central
venous pressure, systemic arterial pressure, and electroencephalogram as clinically indicated.
Cerebral Hemodynamic Monitoring
The Brain Injury Research Center protocol included daily evaluation
of blood flow velocities in all basal arteries of the brain, jugular bulb
oxymetry, and CBF measurement by means of the 133xenonclearance technique. Initial evaluation was obtained as soon as
possible after each patient’s admission to the intensive care unit.
CBF Measurements
CBF measurements were performed according to a technique described previously.6 – 8 In brief, 20 to 30 mCi of gaseous 133xenon
dissolved in normal saline was injected. Thereafter, the cerebral
clearance curves were recorded for 11 minutes at the patient’s
bedside from the area over the estimated scalp projection of the
middle cerebral artery supply territory by 8 NaI detectors connected
to a portable unit (Cerebrograph Cortexplorer 16, Ceretronix). The
data obtained were then extrapolated to 15 minutes, after referencing
the cerebral clearance curve of 133xenon to the clearance curve of
exhaled end-tidal 133xenon, which was used as an estimate of arterial
concentration. As previously described,9 a 2-compartment, modified
height-over-area method7,8 was then used to calculate the hemispheric CBF (derived from 8 ipsilateral detectors) and global CBF
(from all detectors). CBF represents the mean flow of fast- and
slow-clearing compartments, because it is more stable than a
single-compartment method in pathologic situations, especially in
trauma. Ancillary parameters necessary for further calculations of
cerebral hemodynamics and metabolism indexes such as hematocrit,
hemoglobin, and arterial and jugular venous blood gases were
simultaneously recorded.
BFV Measurements
According to a recently described technique,5 ICA BFV measurements were acquired with the use of an angle-independent dual-beam
Doppler ultrasound device (FlowGuard, Cardiosonix Inc). Both
beams are pulse-wave range-gated with sample volumes ⬍200 ␮m
in length. Hundreds of sample volumes are simultaneously analyzed
by digital Doppler along each ultrasound beam. Full fast Fourier
transform analysis for each sample volume and application of an
original algorithm allow real-time detection of flow velocity in the
set of successive gates, followed by determination of the chord
segments that each beam traverses within the blood vessel (Figure 1).
Because the angle between the 2 beams is known, the insonation
angle for each ultrasound beam can be drawn from simple calculation based on trigonometric and Doppler considerations. Further
processing of the large number of small sample volumes allows
determination of the pulsatile velocity profile and vascular diameter.5
Determination of the insonation angles allows, in return, calculation
of absolute BFVs, so that BFV can be directly obtained through
integration of the velocity profile across the vascular cross-sectional
area.
Insonation of the ICA was performed slightly below the jaw near
the mandibular angle with the patient in a supine position with slight
rotation of the head. BFV measurements were made in all patients
immediately before CBF measurements by an operator blinded to the
results of CBF measurements.
Statistical Analysis
Comparison between BFV and CBF values was performed by linear
correlation analysis with commercially available software (NCSS
2000, Number Cruncher Statistical Systems).
Results
Overview
A total of 42 hemispheric CBF measurements were made in
19 patients and 4 volunteers, ranging from 1 to 6 measurements in a single subject. In 2 patients, CBF could not be
obtained from 1 hemisphere, so that 82 hemispheric CBF
values were eventually recorded. These hemispheric CBF
1878
Stroke
August 2003
value of 82.6% (sensitivity 73.3%, specificity 95%). With 30
mL · min⫺1 · 100 g⫺1 used as a threshold value for the
definition of ischemia,10 a BFV of 180 mL/min would be
indicative of ischemia in 4 of 5 patients (sensitivity 66.7%,
specificity 96.6%; positive predictive value of 80%; negative
predictive value of 93.3%). Conversely, BFV sensitivity and
specificity were 60% and 96%, respectively, for the diagnosis
of hyperemia, as defined by a CBF ⬎55 mL · min⫺1 · 100 g⫺1
(positive predictive value of 85.7% and negative predictive
value of 85.7%).
Discussion
Figure 2. Correlation between ICA BFV (mL/min) and ipsilateral
hemispheric CBF (mL · min⫺1 · 100 g⫺1). According to linear correlation analysis, hemispheric CBF could be defined as equal to
ipsilateral (BFV⫻0.0928)⫹14 (r⫽0.76, P⬍0.0001).
Downloaded from http://stroke.ahajournals.org/ by guest on June 16, 2017
values could be compared with only 77 BFV measurements,
because BFV could not be obtained on 1 side in 5 patients
(failure rate of 6%). Failure was related to an unacceptable
difference in either vessel diameter or BFVs, as measured by
the 2 ultrasound channels of the dual probe.
CBF and BFV Correlations
Hemispheric CBF values showed a close and linear correlation with BFV measurements (Figure 2). The correlation
factor was 0.76, with a value of P⬍0.0001. Global CBF
values showed a higher correlation with the total BFV
obtained from both ICAs (Figure 3; r⫽0.84, P⬍0.0001).
With the slope and intercept values obtained from the linear
correlation analysis between CBF and BFV, global CBF
could be derived from BFV from the equation global
CBF⫽(average BFV⫻0.108)⫹10.5. Differences between
calculated global CBF and measured global CBF ranged
between 1.2% and 32.4%, with a mean difference of 14.5%.
Ischemia and Hyperemia Prediction
With 37 mL · min⫺1 · 100 g⫺1 used as the cutoff value for the
ischemic range, a BFV value of 220 mL/min would yield a
positive predictive value of 91.7% and a negative predictive
Figure 3. Correlation between bilateral ICA BFV (mL/min) and
global CBF (mL · min⫺1 · 100 g⫺1). According to linear correlation analysis, global CBF could be defined as (average
BFV⫻)0.108⫹10.5 (r⫽0.84, P⬍0.0001).
Several authors have suggested the implementation of Doppler ultrasound technology for the assessment of BFV in the
ICA as a correlate for CBF in the corresponding cerebral
hemisphere.11–14 Most studies have been based on the use of
spectral Doppler imaging and have mostly reported on BFV
in healthy subjects.11–14 However, the accuracy of spectral
Doppler imaging has been repeatedly challenged, and welldocumented errors in the assessment of BFV have been
reported in the literature.15–17 Recently, Ho et al18 have
emphasized the poor correlation obtained between BFV, as
measured by spectral Doppler imaging, and magnetic resonance phase-contrast flow quantification and have further
supported a previous statement made by Licht et al17 concerning the inaccuracy of spectral Doppler imaging, which
prevents clinicians from drawing therapeutic conclusions by
relying on this technique only. The reasons for the relative
inaccuracy of spectral Doppler imaging are well known and
inherent to the technology itself, based on data acquired from
a single frame. As such, it will most likely generate significant errors in measurements of both velocity and diameter
used for flow calculation. Flow velocity is currently assessed
by Doppler shift, which implies an accurate knowledge of the
insonation angle.15,16 Although sonographic imaging modalities provide for calculation of this angle, errors in its
determination have been reported. Moreover, significant variations in flow velocity are not taken into consideration in
flow calculation. Even though spatial variations in flow
velocity within the vessel lumen are supposed to be integrated
by a sample volume that encompasses the entire cross section
of the vessel, this integration does not take into consideration
the imperfect uniformity of insonation,19 nor the substantial
variations in velocity profile during the cardiac cycle.20 Most
important, variations in vessel diameter as large as 10% occur
during the cardiac cycle21 and are obviously overlooked by
the use of a single frame. This might result in a 20% error in
flow calculations under physiologic conditions22 and an even
larger error in clinical situations associated with increased
pulsatility of the ICA, such as increased peripheral cerebral
vascular resistance. To cope with these shortcomings of
spectral Doppler imaging, color-velocity imaging has been
applied to BFV measurements, because this technology
allows integration of temporal variations of flow velocity and
vessel diameter.23 This technique, however, does compute the
velocity profile and its variations during the cardiac cycle,
which might lead to inaccuracy in BFV measurements. In a
comparative study with magnetic resonance phase contrast,
spectral Doppler, and color-velocity imaging, Ho et al18
Soustiel et al
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showed improved accuracy in BFV evaluations by colorvelocity imaging, although these investigators admitted that
there was poor agreement between magnetic resonance phase
contrast and any other ultrasound technique.
In a recent report, angle-independent dual-beam technology combined with digital Doppler proved to achieve highly
accurate flow volume measurements made in a phantom
model5 and reproducible and reliable BFV evaluations in
healthy subjects. These combined technologies allow the
integration of spatial and temporal variations in both vessel
diameter and BFV, resulting in improved accuracy. In the
present study, BFV evaluations made in the extracranial
segment of the ICA demonstrated a close correlation with
CBF measurements made by a “gold standard” technique, the
133
xenon-clearance technique. When global CBF was considered for analysis, an even closer correlation was found with
the summed BFV values from both ICAs (r⫽0.84). This
closer correlation might be explained in part by the fact that
assessment of CBF by means of BFV does not take into
consideration extracerebral blood flow supplied by ICAdependent vessels, such as the ophthalmic arteries and intracavernous branches of the ICA. More important, intracranial
redistribution of blood flow from the ICA through the
anterior and posterior communicating arteries cannot be
evaluated extracranially and might represent an inherent
source of error. Consequently, assessment of global CBF by
means of bilateral ICA BFV is likely to be more accurate than
hemispheric CBF. In addition to these considerations, when
analyzing correlations between BFV with any gold standard
of CBF measurement, one should keep in mind the difficulty
that exists in accurately measuring CBF and the subsequent
wide spectrum of values in the literature for normal CBF,
ranging from 39 to 69 mL · min⫺1 · 100 g⫺1.24 –27 These
disparities are not limited to those yielded by comparing
different type of modalities but do actually exist between
different studies based on the same technology. As with other
modalities of CBF measurement, the accuracy of the
133
xenon-clearance technique is limited by several technical
shortcomings that might have an influence, especially under
ischemic conditions.28 Among these, various methodological
shortcuts that correct for dispersed arterial input function and
contamination from extracranial tissue might account for the
relatively wide range of reported results. In addition, crosscontamination from the opposite hemisphere might result and
reduce side-to-side differences, which might partly account
for the larger differences noted between hemispheric CBF
and unilateral BFV values when compared with the global
results in this study.
Nevertheless, the results of the present study show that
ICA BFV can be reliably measured and monitored in critically ill patients, with a close correlation with CBF values. In
this series, a BFV ⬍220 mL/min was found to be indicative
of an ischemic trend in 11 of 12 instances (positive predictive
value of 91.7%, specificity 95%) and of mild or severe
ischemia in 4 of 5 patients with a BFV ⬍180 mL/min
(positive predictive value of 80%, specificity 96.7%),
whereas a total BFV value ⬎460 mL/min accurately ruled out
ischemia in 19 of 24 cases (negative predictive value of
82.6%). However, it should be kept in mind that despite the
CBF Assessment by Means of BFV Measurement
1879
demonstrated correlation between reduced BFV in the ICA
and impaired CBF in the corresponding cerebral hemisphere,
no firm conclusion should be drawn regarding tissue outcome
prediction without complementary data, such as cerebral
blood volume (CBV).29,30 Magnetic resonance imaging studies have indeed suggested that CBV is more predictive of
tissue outcome than is CBF in cerebral occlusive disease,29 as
ischemic regions with reduced CBV were shown to be at
higher risk of infarction.30 CBV, however, cannot be estimated by relying on CBF data alone, because the correlation
between CBF and CBV is variable in ischemia.30
Nevertheless, these findings suggest that in patients with
unstable cerebral hemodynamics, BFV measurements might
be of clinical value as a bedside noninvasive tool that can be
repeatedly performed as clinically indicated with a reasonable
margin of error. Special care, however, should be given to
elderly patients and those carrying a high risk of cerebral
vascular occlusive disease. Although several authors have
reported on the clinical value of BFV assessment in extracranial ICA stenosis by color-velocity imaging Doppler,31,32 the
accuracy of those measurements is likely to decrease in such
instances. A localized stenosis, if overlooked by the ultrasound beams, might result in miscalculation of the diameter,
with an overestimation of the BFV. Although repeated
measures with the use of different angles, along with an
insonation target located as high as possible above the carotid
bifurcation, might help reduce the probability of such an
error, duplex assessment of the ICA before monitoring seems
to be indicated in patients at high risk of extracranial vascular
disease. Intracranial carotid stenosis, though less common,
might represent another possible source of error in CBF
estimation, as part of the flow to the corresponding cerebral
hemisphere might be supplied by the opposite ICA or even
the posterior circulation, in some instances. In such situations,
discrepancy between BFV and CBF values should be expected on the same side. Accumulating experience, leading to
improved skills and expertise with this new technology,
should help improve the accuracy of CBF estimations and
further define the place of this modality within the spectrum
of neuromonitoring.
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Assessment of Cerebral Blood Flow by Means of Blood-Flow-Volume Measurement in the
Internal Carotid Artery: Comparative Study With a 133Xenon Clearance Technique
J.F. Soustiel, T.C. Glenn, P. Vespa, B. Rinsky, C. Hanuscin and N.A. Martin
Downloaded from http://stroke.ahajournals.org/ by guest on June 16, 2017
Stroke. 2003;34:1876-1880; originally published online July 3, 2003;
doi: 10.1161/01.STR.0000080942.32331.39
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