Measurement of Carotid Blood Flow in Man and its Clinical

Measurement of Carotid Blood Flow in Man
and its Clinical Application
SUMIO UEMATSU,
M.D.,*
ANDREW YANG,
RICHARD KOUBA,
R.T.,*
M.S.,t
AND THOMAS
THOMAS
J. K.
J.
TOUNG,
PREZIOSI,
M.D.,t
M.D.§
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SUMMARY With the use of a new ultrasonic volume flow meter (VFM), over 8000 measurements of
common carotid blood flow were made in 120 normal control subjects and 550 patients with various
neurological disease. The accuracy of the flow meter in measuring blood flow on an experimental model
ranged from 93 to 97%.
In normal subjects, common carotid bloodflowvaries with age. It increased from newborn to age 20 and
gradually decreased thereafter. In normal healthy subjects, the flow varies within ± 6.7% (2SD) at one
sitting (intrasession) and ± 21.2% (2SD) from week to week (intersession study). Carotid bloodflowvaries
linearly with P a C0 2 and increased markedly in response to endotracheal intubation. In healthy adults, the
flow ratio between the two common carotid arteries is 1.07 ± 0.052. This ratio increases in patients with
transient ischemic attacks to 1.28 ± 0.23 (p < 0.05) and in patients with intracranial space occupying
lesions to 1.46 ± 0.39, (p < 0.01).
In 26 consecutive cases of carotid endarterectomies, the preoperative common carotid blood volume flow
was 5.1 ± 1.0 cc/sec. AH cases preoperatively had at least 30% stenosis and ranged from 30 to 100%
stenosis. The carotid blood volume was significantly increased post-operatively (p < 0.001). The overall
accuracy in detecting carotid and cerebral arterial disease is 89% with sensitivity of 96% and the specificity
of 71%.
Our clinical experience indicates that this device is not only a valuable noninvasive diagnostic tool for
evaluation of carotid disease but also appears to be useful in assessing cerebral blood flow.
Stroke, Vol 14, No 2, 1983
ULTRASONIC DOPPLER FLOW METERS have
been used extensively in recent years in the evaluation
of the hemodynamics of the vascular system. However, the currently routinely used devices have not
been able to determine the actual amount of blood flow
in cc/sec. In our previous paper, we have reported the
accuracy of a new Doppler device, the transcutaneous
Doppler Volume Flow Meter-VFM, in measuring the
actual flow in cc/sec on an experimental model.' In this
paper we summarize our experiences in the use of this
device in assessing common carotid blood flow in various clinical states.
Principle
The device was developed by Furuhata and his coworkers with collaboration of Hayashi-Denki Co.,
Kawasaki, Japan in 1978.2 An A-mode transducer is
used to measure the diameter of the pulsating artery in
real time, and "an angle-independent" Doppler ultrasound technique to measure the velocity of blood flow
at a cross-section of the common carotid artery.2-3 The
diameter is measured and tracked by a phase-locked
echo-tracking method.4 The operator selects a point in
the A-mode echo of the artery wall and moves a tracking gate to coincide with it. The tracking gate will then
lock onto and track the motion of a single cycle from
the echo of the wall of the artery. The diameter of the
pulsating artery is calculated every 2 msec from the
distance between two tracking gates. The system is
capable of measuring arteries 2 to 30 mm in diameter at
a depth of 3-70 mm, with a resolution of 0.5 mm. 1 - 5
In order to measure the true diameter of the artery,
the angle of the sound beam of A-mode has to be
maintained at 90 degrees relative to the longitudinal
axis of the artery. This is accomplished by having the
echo from the vessel wall register on the cathode ray
tube (CRT) only if the incident angle is within ± 5
degree from the desired 90 degree.1-5 A carrier frequency of 5 MHz at 10 KHz repetition rate is used for
the Doppler probe. A sharp cut-off crystal filter extracts the Doppler frequency band of interest. The
band-width of the crystal filter limits the velocity range
of this device to between 9 and 105 cm/sec.
The received values are processed by a built-in computer to calculate the volume of blood flow. The Volume Flow Meter (VFM) provides a CRT, a hardcopy
analog and a digital display of the data. The data consists of mean and range of flow (cc/sec) and velocity
(cm/sec) and range of wall motion of the artery (mm),
in real time and averaged across 5 heartbeats.5
Previously, the uncertainty of the angle between the
probe and the blood vessel has prevented accurate flow
measurements with the Doppler Techniques. The new
device circumvents this problem by deducing the true
velocity using a probe with a known fixed angle between two receiving transducers and a transmitting
transducer. The mathematical formula derived is
shown in figure 1.
From the *Department of Neurosurgery, tDepartment of Biomedical
Engineering, tDepartment of Neurology, §Department of Anesthesiology and Critical Care Medicine Johns Hopkins University, School of
Medicine.
Address correspondence to: Sumio Uematsu, M.D., Johns Hopkins
Hospital, 600 Wolfe Street, Baltimore, Maryland 21205.
Received May 12, 1982; revision accepted October 11, 1982.
Reliability of the Device on Experimental Models
(1) Comparison with Electromagnetic Flow Meter
(EMF)
(A) Static Flow. In a series of experiments carried out
in a model system the volume flow meter described
above was compared with flow measurements ob-
MEASUREMENT OF CAROTID BLOOD FLOW IN MAN/Uematsu et al.
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5 READINGS PER DATA POINT
MEAN + 1 SD IS SHOWN
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CORRELATION COEFFICIENT R- .99
LINEAR REGRESSION Y -1.005X + .136
IN 2-18 CC RANGE Y » .980X + .008
STANDARD ERROR OF ESTIMATE .004
I
1
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tained with an electromagnetic flow meter. Blood flow
was recorded simultaneously by the VFM and the EMF
through teflon tubes with diameters of 2 mm., 5 mm.
and 8 mm. The ratio between the VFM and EMF was
1.05 ± 0.034. The correlation coefficient was + 0.99
(p < 0.001).'
The distance between the transducer and the tube in
the water tank was then varied from 5 mm to 45 mm.
Over this depth range the mean ratio of VFM/EMF was
1.03 (range 0.95 to 1.06). The effect of the angle
between the Doppler transducer package and the axis
of the flow was evaluated. It was found to be accurate
within 10% over a 40° range.
(B) Physiologically Pulsatile Flow. A by-pass between
the abdominal aorta and the inferior vena cava in an
anesthetized dog was used. VFM/EMF ratio for the
pulsating arterial specimen was 0.98. The correlation
coefficient was 0.94 on the 5 mm diameter artery. A
similar high ratio and coefficient were observed on an
8 mm vessel and the irregular branching iliac and abdominal artery.1
(2) Actual Flow Measurement by Constant Flow Pump
Human blood sample from a blood bank was
pumped through a Teflon tube (2 and 5 mm in diameter) by a constant flow pump. The transducer of the
VFM was placed 15 mm away from the tube to monitor
the flow. Five hundred to seven hundred cc of blood
was pumped from one graduated cylinder to another.
Based on the time required to transfer the known
amount of blood, the actual flow rate was calculated.
The ratio between the value of the VFM reading and
the actual flow is shown in figure 2. With the 5 mm
tube, the ratio was nearly one to one. Flow was adjusted in incremental amounts from 2 to 18 cc/sec. The
VFM value was 2% lower with a standard error of
_
ft .
4
FIGURE 1. Schematic diagram of probe and device to measure volumeflow.The probe consists of four piezoelectric transducers. An A-mode transducer measures the diameter of the
artery. Rb., T. and Ra. are Doppler transducers and determine
the velocity of the blood flow. These values are processed by a
built-in computer to calculate the volume of the blood flow in ccl
sec, using the formula shown in the diagram.
-
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10
12
14
16
18
20
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TRUE FLOW CC/SEC
IN-VITRO CALIBRATION 5mm TUBE
FIGURE 2. Comparison between VFM flow readings and true
flow measurement by constant flow pump. A known volume of
blood specimen was transferredfrom one graduated cylinder to
another by a constant flow pump through a 5 mm teflon tube.
The flow reading by VFM and the actual amount of blood
specimen collected in the cylinder correlated well.
0.4%. The ratio was higher in flows of under 2 cc/sec
and over 18 cc/sec. We repeated the experiment for
flows of less than 2 cc/sec using a 2 mm tube to obtain
velocities comparable to newborns whose average artery diameter is 3 to 4 mm. There was a static error of
11% and a coefficient error of 22%. However, the
correlation coefficient was 0.99. 6 - 7
Materials and Methods
1. Subjects
A total of 670 cases were studied. Of these, 120
were normal subjects from newborns to over 60 years
of age and the remaining 550 cases were patients with
various neurological conditions, such as peripheral
nerve disease, intracranial lesions, transient ischemic
attacks (TIAs) and extracranial vascular diseases. The
examination was carried out with the subject relaxed in
a supine position. A transducer was placed over the
common carotid artery one to two finger breadths
above the upper edge of the clavicle. After setting the
gates on optimum near and far side wall echoes of the
artery and obtaining good quality velocity waves, the
computation switch was activated (fig. 3).
2. Variability of the Common Carotid Blood Flow
Serial intrasession (at one sitting) variability and
intersession (week to week) variability and left and
right difference in flow was evaluated in 5 normal
volunteers.
The mean and standard deviation was calculated
from the 5 readings taken on each common carotid
artery. All the data was then normalized using the
subject mean reading as " 1 . 0 0 . " From this the standard deviation of all the data was calculated. This is the
standard deviation of all the subject's data expressed as
STROKE
258
VOL
14,
No
2,
MARCH-APRIL
1983
looping, obvious plaque or narrowing resulting in less
than 20% reduction in the diameter of the internal
carotid arteries.
DIGITAL DISPLAY
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(2). Criteria for Abnormal Volume Flow Measurement
(A) Primary Criteria, a) Less than 6.0 cc/sec of common
carotid flow per side, b) High to low flow ratio between the two carotids greater than 1.20. c) Excessively high mean volume flow (over 15 cc/sec) with greater
than 30% fluctuation in the flow.
(B) Secondary Criteria, a) Irregular velocity wave form,
b) Mean velocity higher than 20 cm/sec. c) Over 30%
decline of carotid flow upon compression of the ipsilateral superficial temporal and facial arteries, d) Velocity less than 10 cm/sec. e) Arterial diameter of greater
than 9.0 mm.
When any of the primary criteria, or two of the
secondary criteria are observed the test is defined as a
positive. A positive secondary criterion occuring alone
may identify technical errors.
Results
1. Normal Control
FIGURE 3. A view of the VFM examination in a laboratorysetting. A probe is placed over the common carotid artery just
above the clavicle (below the carotid bifurcation). After obtaining good arterial wall echoes and velocity waves on the CRT,
the switches for measurement (1), computation (2) and printout
(3) are pressed.
a percent of the mean ("intrasession variability").
The mean carotid flow of each side of the patient
was calculated. Each patient returned for six sessions
over a 3 week period. The six means from the six
sessions were averaged to give a mean for each patient.
This was then normalized to " 1.00" and all the other
means were expressed relative to that value. The standard deviation of the 6 session's mean value was then
calculated ("intersession variability"). Calculation of
the correlation between the left and right side in six
sessions was made for each patient. This was then
averaged to give a correlation coefficient for the entire
group.
The effect of P a C0 2 on the carotid flow was evaluated under general anesthesia on 14 cases during surgery, for spinal disease, depth electrode implantation
or peripheral nerve decompression.
3. Criteria for Interpretation of Angiogram and VFM
(]). Angiographic Criteria for Abnormality
(A) Carotid Stenosis. More than 40% reduction of the
diameter of the carotid artery measured in either of two
planes at the level of the most severe stenotic area
compared to the nearest normal portion of the artery.
(B) Cerebral Arteriosclerosis.
U n e q u i v o c a l r e d u c t i o n in
the diameter of major cerebral (the anterior and middle
cerebral) arteries due to spasm, vasculitis or atherosclerosis with or without retrograde flow.
(C) Abnormal
Carotid Artery Other Than Stenosis.
Severe
(1) Variation With Age
In the 32 newborns with age of 2.9 ± 2.3 days the
volume flow was 1.6 ± 0.46 cc/sec. The flow then
increased to an average of 3.9 ± 0.5 cc/second at one
month and to 7.4 ± 0.3 cc/sec at three years. The
blood flow reaches the highest level between 5 to 20
years of age with a mean of 8.5 ± 1.3 cc/sec. The flow
begins to decline thereafter. From 21 to 40 years of age
the flow is 7.99 ± 1.5 cc/sec. In the 40 to 60 years age
group the mean flow is 7.21 ± 1.15 cc/sec while in the
group of age over 60, it decreased to 6.7 ± 0.49 cc/
sec. The overall range of acceptable normal values for
flow was 6 cc/second to 11 cc/second over the age
range of 5 to over 60 years (table I).
(2) Reproducibility
(A) Intrasession Reproducibility:
T h e Standard d e v i a t i o n
of repeated intrasession measurement was 3.8%. This
indicates that if a patient has repeated readings on one
side, he will have a reading that could be within plus or
minus 7.6% (2SD) variation.
(B) Intersession Reproducibility — The Standard deviation was 10.6%. This indicates that if a patient is
tested on different days from week to week, his readings could fluctuate over a range of ± 21.2% (2SD)
from the average flow. However, even with this fluctuation the flow remains within the normal range of flow
of 6 cc/sec to 11 cc/sec (fig. 4).
(3) Side to Side Flow Variation and Ratio
The high to low flow ratio between the two carotids
was 1.07 ± 0.052. Correlation between the left and
right side between sessions was calculated to see if the
variations were due to a symmetric change in cerebral
blood flow or due to lateralized changes. The relatively
low correlation of 0.63 suggested that both occur.
There were no consistent left to right differences in
flow.
MEASUREMENT OF CAROTID BLOOD FLOW IN MAN/Uematsu et al.
259
TABLE 1 Common Carotid Artery Flow Parameters With Normal Control Subjects
Age
(years)
Normal control
Newborn
(2.9 ± 2 . 3 days old)
Mean flow cc/sec
No.
(L)
(R)
High to
low flow
rate
Wall motion
Mean
diameter
(L)
(R)
32
1.6±0.46
1.6±0.30
1.03
3.9±0.65
0.20 ± 0 . 2 2
0.16±0.09
5-20
11
8.5 ±1.30
8.5 ±1.28
1.07±0.07
6.7 ± 0 . 6 4
0.66 ± 0 . 0 8
0.60±0.16
21^0
16
7.99 ± 1 . 5
7.67±1.3
1.07 + 0.13
7.2±0.50
0.40 ±0.12
0.38±0.11
41-60
14
7.21 ±1.15
7.48± 1.10
1.10 ±0.07
7.5 ±0.77
0.36 ± 0 . 0 9
0.37±O.ll
5
6.7 ± 0 . 4 9
6.6+1.30
1.09 ± 0 . 0 5
7.16±0.65
0.26 ± 0 . 0 6
0.26 ± 0 . 0 9
7.05 ± 0 . 4 9
0.55 ± 0 . 2 0
0.56±0.19
7.5 ± 0 . 5 0
0.53 ± 0 . 0 6
0.44±0.15
61-over
Subnormal control
Post partum
( 2 4 ± 5 y.o.)
30
6.9±1.0
6.4± 1.1
1.08+1.1
Peripheral nerve and
spinal disease
(41 ± 1 3 y.o.)
12
8.5±1.3
8.2±0.60
1.04 ±0.05
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(4) Physiological Variation
(A) Hyper and Hypoventilation and Sit-up Exercise. Com-
mon carotid blood flow was monitored before, during
and after hyper and hypoventilation and sit-up exercises. Hyperventilation tended to lower carotid flow in
all of the cases. However, hypoventilation or exercise
did not cause significant change in 5 subjects without
evidence of cerebral, cardiovascular, or intracranial
diseases. In a typical response from a 30 year old
female, the flow decreased from 9.6 cc/sec to 4.67 cc/
sec within 10 deep rapid respiratory cycles. The flow
rapidly returned to baseline at the cessation of
hyperventilation.
(B) With Response to Controlled Ventilation Changes. The
common carotid blood flow was monitored at an average of 4 readings per minute, and arterial blood gases
determined in 6 patients without clinical evidence of
carotid or cerebral arterial disease during general anes-
thesia. At the lowest P a C0 2 of 17 torr, the carotid flow
decreased from baseline value of 9.0 cc/sec to 5.3 cc/
sec and at the highest P a C0 2 of 49 torr the flow reached
12.02 cc/sec. The correlation coefficient between
P a C0 2 and carotid flow is between 0.777 and 0.929.
The response of carotid blood flow to P a C0 2 is indicated by the slope of the regression line (fig. 5).
(C) In response to endotracheal intubation. The common
carotid blood flow, in general, is relatively stable during the course of general anesthesia, except during
intubation. Flow is markedly elevated (double to triple
baseline value) in response to the endotracheal intubation (fig. 6). Frequently used pharmacologic agents
such as sodium pentothal, and neuromuscular blocking
agents do not change flow significantly. However,
sodium nitroprusside induced hypotension produced
an unexpected increase in carotid flow, as measured by
the VFM within the range of autoregulation.
2. Patient Controls (without cerebrovascular pathology)
(1) Other neurological disease
Twelve patients with peripheral nerve and musculoskeletal disease without any evidence of cerebrovas-
12
cc/sec
432
1
5 N O R M A L RESTING CONTROLS
6 SESSIONS O V E R 3 WEEKS
5 READINGS/SIDE/SUBJECT/SESSION
ITOTAL = 300 READINGS)
M E A N ± 1 SD FOR EACH CCA O F E A C H SUBJECT IS SHOWN
FOR E A C H SUBJECT:
INTRASESSION V A R I A B I L I T Y (2 SD%) = +7.6%
BETWEEN SESSION V A R I A B I L I T Y (2 SD%) = +21.2%
BETWEEN SESSION C O R R E L A T I O N O F L A N D R SIDE R =.63
20-
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FIGURE 4. Variability and reproducibility of the flow in cc/sec
on 5 normal controls. The standard deviation of the mean flow
in one setting was 3.8%. This indicated that intrasession variability could be plus or minus 7.6% (2 SD). The standard
deviation of averaged flow measured between the different days
was 10.66%. This indicates that the flow reading fluctuated ±
21.2% (2 SD).
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FIGURE 5. Regression lines between PjCO^ and carotid flow
on 7 cases during general anesthesia. The correlation coefficients are shown individually. Both values correlated well. The
correlation coefficient ranges from 0.77 to 0.92.
STROKE
260
VOL 14, No 2, MARCH-APRIL
30
H I G H T O LOW F L O W R A T I O I N
UNILATERAL, BILATERAL CAROTID STENOSIS
AND CEREBRAL ARTERIOSCLEROSIS
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3. Patients with cerebrovascular pathology
(1) Carotid and/or cerebral arterial disease
Seventy-seven consecutive patients (154 carotids)
with cerebrovascular symptoms were evaluated with
VFM with reference to volume flow, velocity and flow
ratio. All patients had bilateral biplane carotid arteriograms. The degree and character of the carotid stenosis
was assessed using the above criteria for interpretation
of the angiogram and VFM. Although the statistical
analysis included only cases with greater than 40%
stenosis for purposes of comparison of the flow and/or
ratio to the degree of stenosis, in figures 7 and 8 cases
with 21-40% stenosis were included.
(A) Unilateral. 32 cases had unilateral 20% or greater
reduction in the diameter of the artery, the average was
67.6% (Range: 25% to 100%).
a) Internal carotid
The mean high to low ratio between the two carotids
was 1.3 ± 0.2 in cases with 21 to 40% stenosis, 2.1 ±
0.5 with 41 to 70% stenosis, 2.6 ± 1.5 with 71 to 90%
stenosis and 4.2 ± 3.7 with cases of 91-100% -stenosis
(fig. 7).
The mean volume flow in the common carotid artery
was 6.4 ± 0.7 cc/sec with 21-40% stenosis, 5.7 ±
1.9 with 41 to 70% stenosis, 5.5 ± 1.8 with 71 to 90%
and 3.5 ± 1.8 cc/sec with 91-100% stenosis (fig. 8).
The mean velocity in the common carotid artery was
16.0 ± 5.4 cm/sec with 21^10% stenosis, 10.2 ± 2.5
on 41 to 70% stenosis, 10.7 ± 1.8 with 71 to 90%
stenosis and 2.5 ± 2.7 with 91 to 100% stenosis. The
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(2) In the postpartum period
Thirty subjects averaging 2.4 days post delivery either by spontaneous vaginal or by caesarian section
were studied. There was no statistical difference in the
common carotid flow between the two groups (t =
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Downloaded from http://stroke.ahajournals.org/ by guest on March 23, 2018
cular disease were examined. The mean carotid blood
flow was 8.22 ± 0.60 cc/sec. The high to low flow
ratio was 1.04 ± 0.54. These values were comparable
to the values of an age matched normal control group.
N =5
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FIGURE 6. Increase in carotid flow during intubation (N =
7). Tachycardia and elevation of systemic blood pressure are
usually associated. STP: Pentobarbital. SUX: Succinylcholine.
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UNILATERAL
STENOSIS
FIGURE 7. High to low flow ratio in cases of unilateral and
bilateral carotid stenosis and cerebral arteriosclerosis. Degrees of unilateral carotid stenosis are compared.
degree of stenosis and flow volume was correlated
inversely, as expected with the correlation coefficient
of - 0.73 (p < 0.01).
b) Common Carotid
There was marked fluctuation or abnormally high
velocity (over 20 cm/sec) in all 4 cases with stenosis of
the common carotid artery when the probe was placed
near or at the stenotic site. Zero flow was observed in
two cases of complete occlusion of the innominate
artery.
(B) Bilateral. There were twenty-four cases (48 arteries) in this series. The degree of reduction of the diameter on the higher stenotic side was 86.3% (Range: 5 0 100%) and on the lower stenotic side was 51 % (Range:
26-100%). The mean high to low ratio was 2.4 ± 3.7
(range = 1.06 to 19.79). The mean flow on the more
severely stenotic side was 7.0 ± 4.6 cc/sec, (range =
0.7 to 30 cc/sec) significantly different from age
matched controls (p < 0.01) for both flow ratio and
volume flow. Abnormally high velocity may be registered with as low as 30% stenosis when the probe is
placed near or at the stenotic site. The magnitude of
fluctuation of velocity does not correlate with the degree of stenosis. The degree of reduction of flow or the
flow ratio between the carotids could not distinguish
the grade of stenosis of the carotid artery when the
stenosis was present bilaterally. Some cases had a wide
range of flow fluctuation from a maximum of 95 cc/sec
MEASUREMENT OF CAROTID BLOOD FLOW IN MAN/Uematsu et al.
!EC
261
VOLUME FLOW CC/SEC. ON CEREBRAL
AND CAROTID ARTERY DISEASES
8N'24
SD3.7
Downloaded from http://stroke.ahajournals.org/ by guest on March 23, 2018
I
UNILATERAL
STENOSIS
FIGURE 8. Volume flow in cases of unilateral and bilateral
carotid stenosis and cerebral arteriosclerosis. Degrees of the
unilateral carotid stenosis are compared.
to a minimum of 3 cc/sec. The flow ratio of these cases
ranged from 3.24 to 19.79.
c) Cerebral arteriosclerosis and looping of the
carotid artery
There were 14 cases in this series. The mean flow
ratio was 1.4 (Range: 1.03 - 2.40). The flow on the
lower side was 6.2 ± 1.6 cc/sec and the velocity was
13.2 ± 3.4 cm/sec for the group with cerebral arteriosclerosis or carotid disease with or without carotid
stenosis less than 20%. There was no significant difference in flow ratio or volume flow from age matched
controls (t = 1.59, N.S.). These cases included loops
or kinks or multiple plaques in the internal carotid,
narrowing of the intracranial internal carotid, or major
cerebral occlusions (anterior or middle cerebral artery). There was one additional case of fibromuscular
dysplasia.
FIGURE 9. High to low flow ratio between the two carotid
arteries in a group of normal controls, TIA, postendarterectomy, space occupying lesions, AVM, and cases of carotid
stenosis.
ty cases had unilateral stenosis ranging from 30% to
100%, mean 73 ± 20.5 and 5 cases of bilateral
stenosis ranging 40 to 100%. The preoperative blood
volume flow was 5.1 ± 1.0 cc/sec, and 6 days postoperatively the flow was increased to 8.4 ± 3.6 cc/sec (p
< 0.001). During 3 to 9 months follow up study the
flow did not significantly change (8.8 ± 3.5 cc/sec).
Two cases however, had artificially high flow (17.4 to
22 cc/sec). This finding suggests either severe stenosis
of the common carotid artery or near complete occlusion of the internal carotid artery (fig. 10).
(2) Other cerebrovascular disease (AVM)
There were 2 cases of arteriovenous malformation.
The volume flow was markedly elevated to 11.04 cc/
CAROTID FLOW AFTER ENDARTERECTOMY
d) TIA's without cerebral angiographic
confirmation
In the early phase of this study, nineteen consecutive
cases of suspected TIA were evaluated. The mean age
was 59 ± 10.1. The flow ratio between the two carotids was 1.28 ± 0.4 (2 SD). The normal value for the
same age group is 1.077 ± 0.08 (2 SD) (fig. 9). There
was significant difference from age matched control
(p < 0.05).
e) Follow-up flow study after carotid
endarterectomy
There are 26 consecutive cases for this study. Twen-
'
i .
Operation
30
60
90
120
150 Days
FIGURE 10. Follow-up carotid blood flow study after endarterectomy. Preoperative mean flow was 5.1 ± 1.0 cclsec and
increased to 8.4 ± 3.6 cc/sec at time of discharge.
262
STROKE
8i
7JHH. 195 7828 (24 YEAR OLD FEMALE)
65-
4-
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®
®
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®
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®.®
1
CC/SEC
®®
1-tt-
TIME
PULSE
BP
11:30 A M
124
120/80
131
11:50
DEFIB.
2, MARCH-APRIL
1983
4. Accuracy for assessment of cerebral and carotid disease
CAROTID FLOW (CC/SEC.)
BEFORE AND AFTER RESUSCITATION
ON A CASE OF BRAIN DEATH
\ ®
VOL 14, No
12:20
135
115
150/60
59/36
FIGURE 11. Carotid flow in a case of brain death just before,
during and after resuscitation. The flow of 3 to 4 cclsec is
approximately equal to the flow of the external carotid artery.
DEFIB..defibrillation. O.Normal flow (estimated).
sec (case 19) and 14.2 cc/sec (case 21) on the side of
the malformation as compared to 5.6 cc/sec and 11.4
cc/sec respectively, on the normal side. The high to
low flow ratio was 1.97 and 1.25 respectively.
(3) Space occupying lesions and increased
intracranial pressure
There were 9 cases of space taking lesions. All had
midline displacements on CAT scan due to space occupying lesions. The mean flow on the involved side was
5.1 ± 1.15 cc/sec and the non-involved side was 7.5
± 2 . 9 cc/sec. The high to low flow ratio between the
two carotids was 1.47 (fig. 9). Both value have statistically significant difference from age matched control
values at (p < 0.01).
(4) Brain death
There were 4 cases of brain deaths, of which 3
showed absence of cerebral blood flow by radioisotope
studies. The carotid blood flow was less than 3.5 cc/
sec which is equal to the amount of external carotid
blood flow. Occasionally the flow fluctuated increasing the mean flow to 22 cc/sec representing reflux and
turbulence of internal carotid artery at the base of the
skull.8
In one patient with severe head trauma the blood
flow was recorded before, during, and after cardiac
arrest. The flow steadily decreased to almost zero
when ventricular fibrillation occurred. Immediate resuscitation restored the flow to the prearrest level. Subsequent CAT scan revealed severe brain edema (fig.
11).
The result of the VFM was compared with bilateral
carotid angiogram to evaluate the VFM ability to detect significant carotid stenosis and cerebral or carotid
arterial disease. For statistical purposes the primary
criteria of flow and ratio or combined have been included in the calculations because of their objectivity.
Velocity values and the secondary criteria are supplemental in individual instances but do not enter into or
influence the statistical evaluation of the accuracy of
the VFM. The accuracy of the VFM was defined in
terms of its sensitivity (ability to detect the presence of
disease) and specificity (ability to recognize the absence of disease). Within the framework outlined in
table 2 the results shown in table 3 were obtained. This
table defines the sensitivity and specificity using a
single criterion of either flow or ratio. For purposes of
screening the results obtained were greatest considering flow alone. For purposes of evaluating symptomatic carotid disease, the results were greatest considering
either ratio alone or combining ratio and flow. When
comparing flow alone, we have considered the total
number of arteries. However, for calculations using
ratio between the carotids and the combined data we
have considered the total number of patients (74
patients).
Discussion
This non-invasive flow meter allows simultaneous
measurement of artery diameters by A mode ultrasound and velocity measurements by an angle insensitive doppler technique in the same cross sectional area
to allow the calculation of volume flow in cc per sec.
Dynamic change in flow in cc/sec secondary to emotional change, hyperventilation etc., hence can be
evaluated quantitatively. It further has the capability of
following carotid flow changes occurring in a variety
of disease states affecting the cerebral circulation.
These include focal stenosis of the carotid artery as
well as diffuse decreases secondary to increased intracranial pressure or cerebral arteriosclerosis. Disorders
resulting in significant increase in flow (such as AVM)
can also be detected.
Previously, carotid flow data have been available
only by the use of an electromagnetic flow meter. This
requires surgical exposure of the vessel.9 Our previous
in-vitro experiments have shown a high correlation
between EMF measurements and those recorded by the
VFM. In addition we have documented the accuracy of
the VFM with actual measurements of flow obtained
by a constant flow pump. Other methods of measuring
cerebral blood flow, such as the Xenon isotopic methods, allow measurements of total or regional cerebral
blood flow but not of carotid blood flow. They also
have poor temporal resolution and may not be suitable
for rapid serial studies.
There are several technical criteria which must be
met in order to achieve accurate recordings. These are:
good far and near side echoes from the walls of the
carotid artery, and high quality velocity tracings from
the two receiving transducers on the Cathode Ray Tube
MEASUREMENT OF CAROTID BLOOD FLOW IN MAN/Uematsu
TABLE 2
ANGIOGRAM
RIGHT
LEFT
+
+
+
+
+
+
+
+
Flow
Alone
+
263
Outline Used for Statistic Analysis of the Accuracy
1
1
+ + +|
+|
Ratio
Alone
et al.
INTERPRETATION
True Negative
True Positive
True Negative
True Positive
True Positive
False Positive
False Negative
False Negative
ANGIOGRAM
Downloaded from http://stroke.ahajournals.org/ by guest on March 23, 2018
+
+
+
True Positive
True Negative
False Negative
False Positive
Combined
Abnormal FMow and/or
Ratio With Positive
Angiogram:
True Positive
Abnormal F low and/or
Ratio With Negative
Angiogram:
False Positive
Normal Flo w and Ratio
With Positiv e Angiogram:
False Negative
Normal Flo w and Ratio
With Negative Angiogram
True Negative
(CRT) display during the computation period of 5
heartbeats. Sufficient coupling gel should be used. An
experienced operator can easily locate the common
carotid artery. At least four flow determinations are
taken for each patient to assure reproducibility of the
readings. The device is simple to operate and the results are immediately available. Our normal values for
the common carotid flow for newborns and adults correspond well with published values obtained by venous
occlusion plethysmography,10 electromagnetic flow
meter9 and Xe 133 clearance technique. "•12 Total cerebral blood flow in man, as reviewed in many literature
sources, average 54 mls/min/100 g brain tissue.13 With
an average brain weight of 1400 g. This is equivalent
to 6.3 cc/sec/side.
The internal carotid to common carotid artery flow
estimates to be 70% and the external carotid flow is
approximately that of vertebral flow (30%). Hence,
common carotid arteries flow which this device measures indirectly, represents cerebral blood flow. It
should be pointed out however, that our comparison to
cerebral blood flow figure in literature3"17 is limited by
the availability of accurate data relating common carotid flow to cerebral blood flow.
Our data showing a decline of 21 % in the group over
age 60 compared to the 21-40 age/group (8.5 cc/sec/
side to 6.7 cc/sec/side) is close to the 25% drop between ages of 20 to 70 reported by Naritomi et al.18
The large week to week variability in common carotid artery flow suggests that dynamic changes in
cerebral circulation take place even in the resting,
awake, healthy individuals, hence, minor changes in
flow should not be over-interpreted. Our data of plus
or minus 21 % change correlates well with the study by
Obrist et al using 133 Xe inhalation method.12 Similar
large test-retest coefficients of variation have been reported from the internal carotid injection method.19-20
However, Austin et al21 and Prencipe" reported a variation of only ± 14% by intravenous or intracarotid
l33
Xe injection method respectively. Because those
264
STROKE
VOL 14, No
2, MARCH-APRIL
1983
TABLE 3 Four Cases were Excludedfrom this Statistu alysis; Two Arteriovenous Malformation, One Brain Tumor
with Carotid Stenosis, and One with Incomplete Arteric tic Study. This Statistical Analysis was Done Using the Two
Primary Criteria; Flow or Ratio Alone or Combined.
RATIO
ALONE
FLOW
ALONE
COMBINED
51
58
58
TOTAL (A + B + C + D)
15
6
2
74
51
9
30
148
6
7
3
74
OVERALLACCURACY:
(A + D)/(A + B + C + D)
SPECIFICITY: A/(A + C)
SENSITIVITY: D/(B + D)
89%
71
96
74%
85
66
86%
46
95
88%
63%
67%
89
87
89
> 40% STENOSIS WITH ASCVD
TRUE POSITIVES (D)
TRUE NEGATIVES (A)
FALSE POSITIVES (C)
FALSE NEGATIVES (B)
Downloaded from http://stroke.ahajournals.org/ by guest on March 23, 2018
NEGATIVE PREDICTIVE VALUE:
A/(A + B)
POSITIVE PREDICTIVE VALUE:
D/(C + D)
studies did not evaluate short term (intrasession) testretest reliability, it is difficult to differentiate patient
variability from instrument uncertainty.
On the other hand, despite our 21% variability, all
the readings fall within the well defined limits of 6-12
cc/sec range of normal controls. This suggests that
despite the fluctuations, abnormal cerebral vascular
disease may be recognized and that this method is
useful in defining pathological low flow or high flow
states.
In-vitro studies of flow performed on a 2 mm tube
helps to validate its use in infants whose common
carotid arteries are on the order of 3 to 4 mm in diameter. Currently, there is no widely accepted method in
measuring the carotid cerebral blood flows in the infant. The venous plethysmography method of measuring cerebral blood flow is highly dependent on the
compliance of the calvarium, thus making it unsuitable
for use in older children once skull sutures have been
closed.10 In the normals, there is a large increase in
common carotid flow from newborn to age 3.
It has been shown previously that carotid blood flow
is also profoundly affected by the changes in arterial
PaC02 in conscious man as well as under anesthesia.22- 23 Over the range of 17 to 47 torr, carotid blood
flow varies linearly with PaC02. The marked elevation
of carotid blood flow observed with endotracheal
intubation is clinically important. In certain conditions
the volume flow may not be associated with other
hemodynamic changes, such as arterial hypertension
and tachycardia. The rapid rise of the volume flow
may be hazardous to patients with increased intracranial pressure or cerebral aneurysm.
The preliminary results for detection of carotid and
cerebral arterial disease are encouraging. When the
test is used for screening asymptomatic population
with a low incidence of carotid disease, it is preferable
to have a high specificity and a high positive predictive
value to avoid unnecessary arteriography. Therefore,
from our data it is preferable to use the single criterion
offlowalone. Our data indicates withflowalone as the
criterion a specificity of 85% and a positive predictive
value of 87%. On the other hand, if the population has
a high probability of symptomatic carotid disease, high
sensitivity and high negative predictive value are
important to avoid missing clinically important lesions.24"26 Therefore, from our data it is likewise preferable to use the single criterion of ratio alone or the
combined criteria. Our data indicates with ratio alone a
sensitivity of 96% and a negative predictive value of
88%. Using the combined criteria our data indicate a
sensitivity of 95% and a negative predictive value of
67% (table 3). A relatively low negative predictive
value is due mainly to the fact that the carotidflowmay
be lowered by diseases which may not be demonstrable
by carotid angiography. The accuracy of the volume
flow meter is enhanced in our opinion by the additional
use of the secondary criteria as defined above, although, we have not considered these in our statistical
analysis. In particular in the negative case with a high
index of suspicion it has been found that compression
study of the superficial temporal and facial artery is
valuable by identifying a large drop in flow in cases
where there is severe carotid stenosis.
Mean high to low flow ratio increased with the degree of stenosis. The ratio between the group with 41
MEASUREMENT OF CAROTID BLOOD FLOW IN MAWUematsu
Downloaded from http://stroke.ahajournals.org/ by guest on March 23, 2018
to 70% stenosis and over 70% stenosis was statistically
significant (p < 0.001) (fig. 11). The VFM however,
was unable to estimate the precise degree of stenosis in
individual cases. Paradoxically high velocity readings
are frequently seen in complete occlusion of the internal carotid and in brain death. This may be due to
turbulence and flow reflux.8
Cerebral angiography is not necessarily a good standard for evaluating this technique. Fell et al27 noted
that intra and inter observer repeatability in the interpretation of angiograms for low grade carotid stenosis
is low (75% and 57% respectively). In this series to
maintain consistency of the measurements all were
done by a single observer (one of the authors; SU). In
assessing the percent of stenosis, the portion of the
carotid artery that is taken as reference is subjective.
The tortuosity of some carotids makes single plane
angiogram determination difficult. A severely tortuous
or looped artery may have decreased flow due to a kink
in hypotensive or normotensive states. During angiography the high pressure injection of contrast material
may expand the kinked portion and gives the impression of a highly patent artery.
Because the intracerebral arterioles are the dominant
resistance to flow, the human common carotid artery
must be reduced in cross section area to 10-22% before blood flow is reduced.28 The angiogram does not
identify the changes in the small arterioles. Pathology
in the cerebral arterioles may change carotid flow. For
example, Hachinski29 found, using an intracarotid 133
Xe method, a 35% decrease in cerebral flow over controls in a small series of patients with multi-infarct
dementia.
Ultrasonic volume flow determination may be especially useful for the following conditions.
1. Screening patients with symptoms of cerebrovascular disease and asymptomatic patients at risk for
carotid disease, e.g. carotid bruit, strong family history, or hyperlipidemia.
2. Serial monitoring of carotid flow (cerebral blood
flow)
a. in response to vasodilators, changes in blood
gas, pH and blood pressure
b. in head trauma, intracranial bleeding, increased
intracranial pressure or other acute processes affecting cerebral perfusion.
c. in patients undergoing major surgery who may
be at risk for cerebral vascular accidents or relative hypotension from prolonged anesthesia.
d. Follow up study of the endarterectomy patients.
From our preliminary study, we conclude that this
noninvasive ultrasonic flow meter (VFM) is an important advance in the assessment of carotid disease and in
the quantitative physiological studies of carotid hemodynamics and cerebral blood flow.
Acknowledgments
We thank David H. Edwin, Ph.D. Department of Psychiatry the
Johns Hopkins University School of Medicine for Statistical Analysis of
our data in this text, and our special thanks to Ms. Harriet Grossman and
Ms. Madalena Cesenaro for their secretarial help. Also thanks to our
et al.
265
Neurometries technicians Michael Trattner, RT, Fred Wolfe, RT, Erva
Baden, RT, and Jay Wursta, RT, for their technical assistance.
References
1. Uematsu S: Determination of volume of arterial blood flow by an
ultrasonic device. J Clin Ultrasound 9: 209-216, 1981
2. Furuhata H, Kanno R, Kodiara K, et al: Development of ultrasonic
volume flow meter. Proceedings of Japanese Soc Med Engineering
and Biomed. Engineering 2: D. 33, 1978
3. Duck FS, Hudson CJ: A practical method of eliminating the angular dependence of Doppler flow measurements. Abstracts of 10th
ICMBE 15: 1973
4. Hokanson DE, Mozersky DJ, Summer RS, Strandness DE: A
phase-locked echo tracking system for recording arterial diameter
changes in vivo. J Appl Physiolo 32-35: 728-733, 1972
5. Kodaira K, Furuhata H, Shitaji E et al: Development of noninvasive cerebral blood flow meter. Medical Technological Development Foundation (Jap) 95: 1979
6. Uematsu S, Yang A: Transcutaneous measurement of carotid artery volume flow by an ultrasonic device. In IEE. 1981 Frontiers of
Engineering in Health Care B. A. Cohen (ed), IEEE, NY, 154158, 1981
7. Uematsu S, Yang A: Normal and abnormal common carotid artery
blood flow by transcutaneous ultrasonic volume flow meter. In
Noninvasive Assessment of the Cardiovascular System (ed) Edward B. Dietrich, Boston Wright. PSG Inc., 87-96, 1982
8. Uematsu S, Smith T, Walker AE: Pulsatile cerebral echo in diagnosis of brain death. J Neurosurg 48: 866-875, 1978
9. Kristiansen K, Krog J: Electromagnetic studies on the blood flow
through the carotid system in man. Neurol 12: 20-23, 1962
10. Cross KW, Dar PRF, Hathorn MDS et al: An estimation of intracranial blood flow in the newborn infant. J Physiol 289: 329-345,
1979
11. Prencipe: Reproducibility of cerebral blood flow determinations.
Cerebral Blood Flow and Intracranial Pressure, Proc. Fifth Intern,
symp. Roma-siena, 1971, Pt. I.EuropNeuro6:234-235, 1971/72
12. Obrist WD, Thompson HK, Wang HS et al: A simplified procedure
determining fast compartment and cerebral blood flow by '"Xe
inhalation. In Brain and Blood Flow. W Ross-Russell, ed. London:
Pitman, 1971
13. Bloor BM, Glista GG: Observations on simultaneous internal carotid artery and total cerebral blood flow measurements in man.
Neurosurg 2: 249-255, 1977
14. Roberts R, Hardesty WH, Holling HE, Reivich M, Toole JF:
Studies on Extracranial Blood Flow. Surg 56: 826-833, 1964
15. Wood CPL, McKinney WM, Toole JF: Triplanar imaging and
measurement of flow in the vertebral artery with computerized
multichannel pulsed doppler ultrasound. Proceedings of the
AIUM/SDMS Annual Convention Aug. San Francisco 904: 1721, 1981
16. Potter JM: Redistribution of Blood to the Brain Due to Localized
Cerebral Arterial Spasm. Brain 82: 367-376, 1959
17. Obrist WD, Silver D, Wilkinson WE, Hare LD, Heyman A, Wang
HS: The m X e Inhalation Method: Assessment of rCBF in carotid
endarterectomy. In Cerebral Circulation and Metabolism (ed)
Langfitt T et al. Springer-Verlag New York Heidelberg, Berlin,
398-401, 1975
18. Naritomi H, Meyer JS, Sakai F, Yamaguchi F, Shaw T: Effects of
Advancing Age on Regional Cerebral Blood Flow: Arch Neuro36:
410-416, 1979
19. Hoedt-Rasmussen K: Regional cerebral blood flow. The intraarterial injection method. Acta, Neurol Scand (suppl) 27: 1, 1967
20. McHenry LC, Jaffe ME, Goldberg HI: Regional cerebral blood
flow measurements with small probes. I. Evaluation of the method.
Neurol 19: 1198, 1969
21. Austin G, Laffin D, Rouhe S, Hayward W, Rice-Edwards M:
Intravenous isotope injection method of cerebral blood flow measurement: Accuracy and reproducibility in cerebral circulation and
metabolism (ed) Langfitt, TW et al: Springer-Verlag, New York,
Heidelberg, Berlin, 391-393, 1975
22. Kety SS, Schmidt CF: The effects of active and passive hyperventilation on cerebral blood flow, cerebral oxygen consumption, cardiac output and blood pressure of normal young men. J Clin Invest
25: 107-119, 1946
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23. Kreuscher H, Grote J: Effect of hyper and hypoventilation on CBF
during anesthesia. In Brock M, Fieschi C, Ingvar DH et al (eds):
Cerebral blood flow: Clinical and experimental results. New York/
Heidelberg/Berlin: Springer-Verlag, 244-245, 1969
24. Sumner DS: Noninvasive methods for preoperative assessment of
carotid occlusive disease. Part 1. Statistical interpretation of test
results. Vascular Diagnosis and Treatment June/July: 41-54,
1981
25. Krieg AF, Gambino R, Galen RS: Why are clinical laboratory tests
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26. Vecchio TJ: Predictive value of a single diagnostic test in unselected populations. N Engl J Med 274: 1171-1173, 1966
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27. Fell G, Phillips DJ, Chikos PM, Harley JD, Thiele BL, Strandness
D: Ultrasonic duplex scanning for disease of the carotid artery. Circ
64: 1191-1195, 1981
28. Reivich M, Waltz AG: Circulatory and Metabolic Factors in Cerebrovascular Disease. Cerebrovascular survey report for Joint
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and National Heart and Lung Institute, 55-82, 1980
29. Hachinski V: Cerebral blood flow differentiation of Alzheimer's
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(eds): Raven Press, New York, 97-103, 1978
CSF Enzymes in Lacunar and Cortical Stroke
Downloaded from http://stroke.ahajournals.org/ by guest on March 23, 2018
AUSTIN
GEOFFREY
A.
E.
M.D., F.R.A.C.P.,*
DOYLE,
DONNAN,
M.D., F.R.A.C.P.,*t
AND PETER
F.
PETER ZAPF,
BLADIN,
B.Sc.,t
M.D., F.R.A.C.P. $
SUMMARY Cerebrospinal fluid enzyme levels of creatine kinase (CK), lactate dehydrogenase (LDH),
glutamate oxaloacetate transaminase (GOT) and angiotensin converting enzyme (ACE) were studied in 40
acute stroke patients comprising 20 lacunar strokes and 20 cortical strokes. A marked elevation of at least
one of the enzymes CK, GOT or LDH was seen in 80% of cases of cortical stroke. No elevation was seen in
lacunar stroke with CK, GOT or ACE and only a slight elevation with LDH. Within the cortical group, there
was a correlation between the site, size of infarction seen on CT scan and enzyme level.
Thesefindingsmay help to explain the previously noted unpredictability of rises in CSF enzymes in stroke
patients. In certain instances, a study of CSF enzymes may be of use to distinguish cortical from lacunar
stroke. A precise diagnosis of lacunar infarction is important for management purposes, entry into stroke
treatment trials or description of new syndrome types.
Stroke, Vol 14, No 2, 1983
SINCE FISHER AND OTHERS established the five
lacunar syndromes1-5 by careful clinicopathological
correlation, it has become obvious that other conditions may mimic these syndromes.6-8 Cortical infarction8 is the most important of these conditions, since
the pathophysiology of its development is considered
to be embolic and a search for a proximal site of embolization with carotid angiography may be warranted.
This in in contradistinction to lacunar stroke, which is
usually due to small vessel hypertensive disease9 and
angiography is avoided. With the introduction of CT
scanning, it has become obvious that partial lacunar
syndromes frequently exist,10 and it is in this group that
the distinction between lacunar and cortical infarction
may be even more difficult.
This study examines the possibility that the appearance of enzymes in the cerebrospinal fluid (CSF) may
be a useful and simple adjunct to other tests in detecting cortical involvement, thereby assisting in the distinction between cortical and lacunar syndromes. A
review of the current methods of diagnosis of lacunar
infarction is also given and inference about the nature
of release of enzymes into the CSF in stroke is made.
From Austin Hospital, University of Melbourne, Australia, Departments of *Medicine, tBiochemistry and ^Neurology.
Address correspondence to Dr. G. A. Donnan, Department of Medicine, Austin Hospital, University of Melbourne, Australia.
Received June 8, 1982: revision accepted October 12, 1982.
Patients, Materials and Methods
A total of 40 stroke patients were studied in two
groups. The first group comprised 20 consecutive patients with lacunar syndromes in whom the site of
infarction was documented on CT Scan. Further precision of diagnosis was established by the finding of a
normal EEG" and no abnormality on a standard battery of neuropsychological tests.1 The second group
consisted of 20 consecutive patients with 'cortical'
stroke; hemiplegia was accompanied by cortical signs
such as dyspraxia, dysphasia and agnosia, focal abnormality on EEG contralateral to the physical deficit,
abnormalities on neuropsychological testing and confirmation of the site of infarction on CT Scan.
A neurological score was devised for each patient
based on motor and sensory deficit; a score of 0-6 was
given for each of face, arm and leg (motor and sensory)
ranging from no deficit (score, 0) to maximal deficit
(score, 6). Thus maximal deficit involving face, arm
and leg gave a total score of 36.
Lumbar puncture was performed within 48 hours of
admission and estimates of creatine kinase (CK), Glutamic oxaloacetic transaminase (GOT), Lactic dehydrogenase (LDH) and angiotensin converting enzyme
(ACE) were made. ACE was chosen because of its
known concentration in the region of the basal ganglia.12 Total CSF CK has been shown to be almost
entirely brain isoenzyme (CK BB).13 Serum for en-
Measurement of carotid blood flow in man and its clinical application.
S Uematsu, A Yang, T J Preziosi, R Kouba and T J Toung
Downloaded from http://stroke.ahajournals.org/ by guest on March 23, 2018
Stroke. 1983;14:256-266
doi: 10.1161/01.STR.14.2.256
Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 1983 American Heart Association, Inc. All rights reserved.
Print ISSN: 0039-2499. Online ISSN: 1524-4628
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