Doppler Sonography Evaluation of Flow

Velocity and Volume of the Extracranial

Internal Carotid and Vertebral Arteries
in Healthy Adults

Ramazan Albayrak, Associate Professor,1 Bumin Degirmenci, Associate Professor,1

Murat Acar, Assistant Professor,1 Alpay Haktanır, Assistant Professor,1
Mehmet Colbay, Associate Professor,2 Mehmet Yaman, Associate Professor3

1
Department of Radiology, Afyon Kocatepe University, Afyon 03200, Turkey
2
Department of Internal Medicine, Afyon Kocatepe University, Afyon 03200, Turkey
3
Department of Neurology, Afyon Kocatepe University, Afyon 03200, Turkey

Received 30 December 2005; accepted 6 November 2006

ABSTRACT: Purpose. To measure with Doppler so-
nography the velocity and volume of blood flow in the
extracranial internal carotid artery (ICA) and vertebral ar-
tery (VA) of healthy adults and to calculate total cerebral
blood flow volume (tCBFV).
Methods. Bilateral ICA and VA were examined
sonographically in 180 healthy adults. Angle-cor-
rected peak systolic (Vps), end-diastolic (Ved), and
time-averaged maximum blood flow velocity (TAV)
were measured in pulsed Doppler mode, and the re-
sistance index (RI) and pulsatility index (PI) were cal-
culated. The cross-sectional area (A) was measured
on gray-scale images. Volume flow was calculated as
FV ¼ TAV
A, and tCBFV was calculated as the sum
of the right and left ICA and VA volume flow.
Results. tCBFV was 651 6 96 ml/min for the entire
population. There was a significant decrease in Vps,
Ved, TAV, and tCBFV with age in all arteries. RI and PI
values initially declined and then increased with age.
Cross-sectional area increased with age in ICA but not
in VA. PI and RI were higher in men than in women.
Blood flow velocity and volume were higher, and RI
was lower in the left than in the right VA.
Conclusion. The Doppler sonographic assessment
of extracranial ICA and VA blood flow volume may be
useful for the study of cerebral hemodynamic changes
in patients with cerebrovascular disorders. Age-de-
pendent changes should be considered, for instance,
in the management of intensive care patients with
impaired cerebral perfusion. V C 2006 Wiley Periodicals,
Correspondence to: R. Albayrak
' 2006 Wiley Periodicals, Inc.
VOL. 35, NO. 1, JANUARY 2007—DOI 10.1002/jcu
Inc. J Clin Ultrasound 35:27–33, 2007; Published
online in Wiley InterScience (www.interscience.wiley.
com). DOI: 10.1002/jcu.20301
Keywords: cerebral blood flow volume; blood flow
velocity; Doppler; carotid artery; vertebral artery
he ability to assess and monitor total cerebral
T blood flow volume (tCBFV) is clinically im-
portant, particularly in patients with cerebrovas-
cular disorders, serious head trauma, and in-
creased intracranial pressure. Increased intracra-
nial pressure is a common condition in neuro-
logic intensive care units, and reducing tCBFV is
among the therapeutic alternatives,1,2 depending
on whether cerebral hypoemia or hyperemia can
be demonstrated (eg, in patients with meningitis
or subarachnoid hemorrhage). Doppler sonogra-
phy is a noninvasive technique that may contrib-
ute to this diagnosis and reduce the need for scin-
tigraphy in these patients. It may be also be
useful to assess the results of embolization of in-
tracranial arteriovenous shunts. The prevalence
of atherosclerosis, ischemia, infarction, and neu-
rodegenerative disorders increases with age and
causes impairment in cerebral perfusion. Hence,
the age-dependent changes in tCBFV should be
understood and considered. This parameter can
be obtained with Doppler sonography as the sum
of volume blood flow in the left and right internal
carotid artery (ICA) and vertebral artery (VA).3
The main goal of this study was to assess blood
27
 ALBAYRAK ET AL
flow velocity, waveform parameters, and cross-
sectional area of the left and right ICA and VA,
and calculate tCBFV, in healthy adults, and eval-
uate their side and sex differences as well as
their age-dependent changes.
SUBJECTS AND METHODS
One hundred eighty healthy adults (90 women,
mean age, 49.5 6 17.5 years; 90 men, mean age,
49.8 6 17.4 years) were included in the study.
The subjects were divided into 3 groups: 20–
39 years old (group I), 40–59 years old (group II),
and 60–79 years old (group III), with 30 women
and 30 men in each group. None of the subjects
had a history of cardiac, neurologic, or cerebro-
vascular disease. Subjects with atherosclerotic
plaque or stenosis at the site of measurement
were excluded. Informed consent was obtained
from each of the subjects before examination, and
the study was approved by the ethical committee
of our institution.
The examinations were performed in a room
with a comfortable temperature after each sub-
ject had been resting for at least 15 minutes in
the supine position. We used a color-coded duplex
scanner (Nemio 20; Toshiba, Tokyo, Japan)
equipped with a 7.5-MHz linear-array trans-
ducer. The subject’s head was slightly elevated
and turned toward the opposite side by 258 to 408
for ICA measurements and 108 for VA mea-
surements. Measurements were performed 1.5 cm
distal to the carotid bifurcation on the ICA and
between the transverse processes of vertebrae C4
and C5 on the VA. The same radiologist (R.A.)
performed all of the examinations. All measure-
ments were performed at least twice.
The vessel lumen diameter (d) was measured
on a gray-scale image frozen at systole, and the
cross-sectional area of each vessel was calculated
as A ¼ (d/2)2
[p]. Angle-corrected blood flow
velocity was measured with the pulsed Doppler
sample volume expanded to encompass the entire
vessel diameter. Visual control of the maximal
luminal width and acoustic control of an opti-
mum Doppler frequency shift revealed that the
sample volume was centered on the vessel axis.
The angle of insonation was kept as low as possi-
ble (&608). The time-averaged mean blood flow
velocity was automatically calculated by the sys-
tem over 3–5 complete cardiac cycles. Measure-
ments performed on the left and right ICA and
VA were peak systolic maximal blood flow velocity
(Vps), end diastolic maximal blood flow velocity
(Ved), and time-averaged maximum blood flow
velocity (TAV). From these data, the resistance
28
index (RI) was calculated as RI ¼ [(Vps  Ved)/
Vps] and the pulsatility index (PI) was calculated
as PI ¼ [(Vps  Ved) / TAV]. The volume blood
flow (VBF) of each artery was calculated as:
VBF ¼ TAV
A. Cross-sectional area and blood
flow velocity were measured at the same site.
The total cerebral volume blood flow (tCBF)
was calculated as the sum of volume blood flow
values measured in the left and right ICA and
VA. All measurements were documented with a
video printer.
Statistical analysis was performed using SPSS
version 11 for Windows (SPSS, Chicago, IL). Suit-
ability of the sample distribution was tested with
the Kolmogorow-Simirnov test. The Student’s t
test was used to compare data between normally
distributed samples. The Wilcoxon rank test and
the Mann-Whitney U test were used to compare
samples that were not normally distributed to
assess side-to-side and sex differences, respec-
tively. The Pearson correlation coefficient was
used to assess the correlation between volume
flow, flow velocity, and age. All parametric results
are expressed as the mean 6 SD. A P value of
less than 0.05 was considered significant for all
parameters.
RESULTS
The sum of both ICA volume flows was 483 6 79
ml/min (74.2% of tCBFV); the sum of both VA vol-
ume flows was 168 6 52 ml/min (25.8% of tCBFV).
There was no significant difference in tCBFV
between women and men. Flow velocity and vol-
ume were greater in the left than in the right VA
(p < 0.05 for both). Regarding age, tCBFV was 716
6 75 ml/min, 655 6 84 ml/min, and 584 6 80 ml/min
in group I, group II, and group III, respectively
(Table 1). There was a significant inverse correla-
tion between age and tCBFV (r ¼ 0.608, p <
0.0001), left ICA (r ¼ 0.330, p <0.0001), right
ICA (r ¼ 0.384, p <0.0001), left VA (r ¼ 0.320,
p <0.0001), and right VA (r ¼ 0.239, p ¼ 0.001)
volume flow (Figs. 1 and 2). Flow velocity decreased
with age in ICA and VA (p < 0.0001) (Table 2).
Cross-sectional area increased with age in the left
and right ICA (p < 0.05 for both), and was greater
in men than in women (p ¼ 0.09). PI and RI ini-
tially decreased, then increased with age (p <
0.05) (Table 3). Left ICA RI and PI values, right
ICA, left VA and right VA PI values were higher in
men than in women (p < 0.05). VA RI was lower on
the left than on the right side (p < 0.05).
The sum of both ICA, and the sum of both VA, as
well as the right ICA and VA volume flow were
lower in group II than in group I (p < 0.05). The
JOURNAL OF CLINICAL ULTRASOUND—DOI 10.1002/jcu
 CAROTID AND VERTEBRAL ARTERY BLOOD FLOW IN HEALTHY ADULTS

TABLE 1
Blood Flow Volumes (ml/min) in the ICA and VA of Different Age and Sex Groups

Artery Group I (20–39 Years) Group II (40–59 Years) Group III (60–79 Years) Entire Cohort (20–79 Years)

Men LICA 260 6 43 252 6 50 218 6 50 243 6 51

RICA 264 6 37 238 6 41 224 6 50 242 6 46
LVA 103 6 49 88 6 45 73 6 46 88 6 48
RVA 80 6 42 69 6 32 68 6 43 73 6 39
Women LICA 247 6 33 249 6 48 218 6 35 238 6 41
RICA 266 6 43 244 6 59 216 6 50 242 6 55
LVA 106 6 45 93 6 32 75 6 25 91 6 37
RVA 99 6 39 76 6 30 73 6 33 83 6 36

All parameters are expressed as the mean 6 SD. There were 30 subjects in each sex and age group (total ¼ 180).
Abbreviations: LICA, left internal carotid artery; LVA, left vertebral artery; RICA, right internal carotid artery; RVA, right vertebral artery.

sum of both ICA, and the right VA volume flow were

lower in group III than in group II and I (p < 0.05).
In group II, volume flow was higher in the left than
in the right VA (p < 0.05). In the blood flow volume,
there were no differences with regard to sex.
Left ICA Vps, right ICA Vps and Ved, and left
and right VA Vps were lower in group II than in
group I (p < 0.05). Left and right ICA Ved and left
VA were lower in group III than in groups I and
II (p < 0.05). In group I, left ICA Ved and right
ICA Vps and Ved were higher in women than in
men (p < 0.05). In group I, right ICA Vps and
left VA Vps were higher than on the contra-
lateral side (p < 0.05). In group II, Vps and
Ved were higher in the left than in the right VA
(p < 0.05).
Left and right ICA and left VA RI and PI were
lower in group II than in groups I and III. Left
and right ICA and VA RI and PI were higher in
group III than in groups I and II (p < 0.05). In
group I, left ICA and left and right VA PI values
were higher in men (p < 0.05). In group III, left
ICA PI and right VA, RI, and PI values were
FIGURE 1. Age-dependent decrease of tCBFV (r ¼ 0.608, p < 0.0001)
higher in men (p < 0.05). In group II, VA, RI, and in 180 healthy adult subjects (20–79 years).
PI were higher on the left than on the right side
(p < 0.05). The cross-sectional area of the left and
the same technique to measure CBFV in children in
right ICA was greater in groups II and III than in
1957. In 1961, Nylin et al.6 used 32P-labeled eryth-
group I (p < 0.05). In group I, the cross-sectional
rocytes in healthy men. Since then, many methods
areas of the left and right ICA was larger in men
have been used for this measurement.3,7–10
than in women (p < 0.05; Table 4).
CBFV is close to 50 ml/100g/min in healthy
The volume flow was below 30 ml/min in one
adults, and most normal values are in the 45–55
VA in 29 subjects (16.1 %), and it was over 150
ml/100g/min range.11 CBFV declines with age.12,13
ml/min in the contralateral VA in 9 subjects (5 %).
Some sonographic or nuclear magnetic resonance
The left VA volume flow was below 30 ml/min in 10
(NMR) studies have reported an annual CBFV de-
subjects (5.6%), and it was over 150 ml/min in the
crease of 3–4.8 ml/min,14–16 which was not found
right VA in 3 subjects (1.6%).
by other studies using single photon emission CT
or positron emission tomography.17,18 Some inves-
tigators have found no sex differences,14,16 while
DISCUSSION
others have reported a higher CBFV in women.19,20
Cerebral blood flow volume (CBFV) was measured Single photon emission CT and positron emis-
for the first time by Kety and Schmidt in 19484 sion tomography are able to assess regional CBFV,
using nitrous oxide. Kennedy and Sokoloff5 used whereas Doppler sonography can only assess the
VOL. 35, NO. 1, JANUARY 2007—DOI 10.1002/jcu 29
 ALBAYRAK ET AL

FIGURE 2. Age-dependent decrease of left ICA flow volume (r ¼ 0.330, p < 0.0001), right ICA flow volume (r ¼ 0.384, p < 0.0001), left VA flow
volume (r ¼ 0.320, p < 0.0001), and right VA flow volume (r ¼ 0.239, p ¼ 0.001) in 180 healthy adult subjects (20–79 years).

TABLE 2
Blood Flow Velocities (cm/s) in the ICA and VA of Different Age and Sex Groups

Group I (20–39 Years) Group II (40–59 Years) Group III (60–79 Years)

Artery Vps Ved Vps Ved Vps Ved

Men LICA 70 6 22 22 6 5 56 6 14 21 6 5 54 6 17 16 6 6
RICA 69 6 17 22 6 5 54 6 12 21 6 5 55 6 16 17 6 5
LVA 45 6 12 12 6 4 39 6 11 14 6 5 37 6 16 10 6 6
RVA 40 6 11 11 6 3 35 6 9 11 6 3 38 6 16 10 6 4
Women LICA 68 6 14 25 6 4 53 6 11 22 6 6 48 6 11 17 6 5
RICA 79 6 14 27 6 6 53 6 12 20 6 6 48 6 12 16 6 4
LVA 46 6 12 14 6 6 38 6 9 13 6 3 37 6 9 10 6 3
RVA 42 6 10 13 6 4 35 6 9 11 6 4 36 6 8 10 6 3

All parameters are expressed as the mean 6 SD. There were 30 subjects in each sex and age group (total ¼ 180).
Abbreviations: LICA, left internal carotid artery; LVA, left vertebral artery; RICA, right internal carotid artery; RVA, right vertebral artery; Ved, end
diastolic velocity; Vps, peak systolic velocity.

30 JOURNAL OF CLINICAL ULTRASOUND—DOI 10.1002/jcu

 CAROTID AND VERTEBRAL ARTERY BLOOD FLOW IN HEALTHY ADULTS

TABLE 3
Resistance Index and Pulsatility Index of the ICA and VA of Different Age and Sex Groups

Group I (20–39 Years) Group II (40–59 Years) Group III (60–79 Years)

Artery RI PI RI PI RI PI

Men LICA 0.66 6 0.09 1.36 6 0.53 0.60 6 0.09 1.02 6 0.28 0.68 6 0.09 1.27 6 0.33
RICA 0.66 6 0.09 1.40 6 0.59 0.60 6 0.08 1.03 6 0.26 0.67 6 0.07 1.25 6 0.34
LVA 0.70 6 0.08 1.46 6 0.52 0.65 6 0.08 1.15 6 0.29 0.71 6 0.07 1.43 6 0.37
RVA 0.70 6 0.07 1.46 6 0.47 0.67 6 0.07 1.26 6 0.32 0.74 6 0.07 1.48 6 0.29
Women LICA 0.62 6 0.06 1.06 6 0.20 0.59 6 0.08 0.96 6 0.24 0.65 6 0.07 1.10 6 0.22
RICA 0.64 6 0.08 1.18 6 0.33 0.62 6 0.06 1.03 6 0.20 0.66 6 0.06 1.12 6 0.19
LVA 0.68 6 0.08 1.22 6 0.31 0.63 6 0.07 1.07 6 0.26 0.70 6 0.07 1.29 6 0.28
RVA 0.68 6 0.08 1.20 6 0.31 0.68 6 0.07 1.22 6 0.27 0.69 6 0.08 1.29 6 0.28

All parameters are expressed as the mean 6 SD. There were 30 subjects in each sex and age group (total ¼ 180).
Abbreviations: LICA, left internal carotid artery; LVA, left vertebral artery; PI, pulsatility index; RI, resistance index; RICA, right internal carotid
artery; RVA, right vertebral artery.

TABLE 4
Blood Flow Velocities and Cross-sectional Areas in the ICA and VA of Different Age and Sex Groups

Group I (20–39 Years) Group II (40–59 Years) Group III (60–79 Years)

Artery TAV (cm/s) A (mm2) TAV(cm/s) A (mm2) TAV (cm/s) A (mm2)

Men LICA 34 6 8 12.5 6 2.7 34 6 7 12.5 6 2.4 30 6 10 19 6 4

RICA 34 6 6 12.8 6 1.8 32 6 6 12.6 6 2.9 30 6 9 13.1 6 4.9
LVA 22 6 6 7.2 6 2.4 23 6 7 6.1 6 1.7 19 6 9 13.8 6 4.8
RVA 20 6 5 6.7 6 3.1 19 6 4 5.7 6 1.7 19 6 8 5.7 6 2.4
Women LICA 41 6 7 10.4 6 2.2 34 6 8 12.7 6 3.1 29 6 7 5.7 6 2.3
RICA 44 6 7 10.2 6 1.9 33 6 9 13.1 6 4.1 29 6 7 13.3 6 4.3
LVA 26 6 7 6.4 6 2.1 23 6 5 6.7 6 2.2 20 6 5 12.9 6 3.7
RVA 24 6 6 6.7 6 2.1 20 6 6 6.3 6 2.1 30 6 10 6.1 6 1.8

All parameters are expressed as the mean 6 SD. There were 30 subjects in each sex and age group (total ¼ 180).
Abbreviations: A, cross-sectional area; LICA, left internal carotid artery; LVA, left vertebral artery; RICA, right internal carotid artery; RVA, right
vertebral artery; TAV, time-averaged velocity.

relative contribution of the ICA and VA. As soon
as 1943, Dumke and Schmidt21 reported that the
vertebrobasilar system contributed to 30% of
tCBFV in monkeys. In human studies, this ratio
had been reported to be in the 20–24% range.14,22
Several investigators have used Doppler sonog-
raphy for the measurement of tCBFV and the eval-
uation of cerebral hemodynamics.3,14,23,24 The first
of these studies found no age-related change in
tCBFV, ICA or VA diameter, or blood flow velocity
waveform but reported higher diameter and vol-
ume flow in the left than in the right VA.3 In a sec-
ond study, in which age-related changes of cerebral
hemodynamic were reported, only ICA flow velocity
and volume, together with RI, decreased, whereas
PI remained constant and VA diameter increased
slightly with age. The same study reported smaller
ICA diameter in women than in men without side-
to-side difference in flow volume or velocity or in
waveform parameters. This study measured ICA
and VA flow volume but did not calculate tCBFV,24
whereas other studies reported only tCBFV.14,23
To our knowledge, our study has validity
because of the large number of subjects, because
VOL. 35, NO. 1, JANUARY 2007—DOI 10.1002/jcu
we measured blood flow specifically on the left
and right ICA and VA (but not in the common ca-
rotid artery nor the external carotid artery), and
because we calculated tCBFV and evaluated age-
related changes and sex differences in such a
large sample. Our results are in agreement with
previous studies with regard to the effects of age
and sex on tCBFV12–16,23 and age-dependent
changes in flow velocity,24 although another
study reported no significant differences in VA
flow velocities and volume between younger and
older subjects.25 In our study, RI and PI in all ves-
sels except the right VA were lower in the middle-
aged group compare with the younger and older
groups. Unlike previous studies,3,24 we found a
higher PI in the left and right ICA and VA and a
higher RI in the left ICA in men compared with
women. Flow velocity and volume were higher on
the left than on the right VA, without significant
difference in cross-sectional area.
Although our results are in agreement with
data previously reported by others, there may be
some differences because of the way we calcu-
lated blood flow volume and waveform parame-
31
 ALBAYRAK ET AL
ters from the TAV, which is commonly used for PI
and RI calculation, whereas time-averaged mean
blood flow velocity is more commonly used for
blood flow volume measurement. We may argue,
though, that most of the flow occurs during sys-
tole, where the velocity profile is more or less flat
(mean and maximum flow velocity being similar).
During diastole, the velocity profile becomes
parabolic, and the mean velocity is approxi-
mately half the maximum velocity. Therefore, our
method may have resulted in slightly overesti-
mated blood flow volume data.
Volume blood flow measurement is very useful
for clinical studies involving the evaluation of
cerebral hemodynamic changes related to carotid
stenosis, the effect of carotid endarterectomy,
angioplasty and stenting, and various cerebro-
vascular diseases. It may also be useful for cere-
bral blood flow monitoring, the assessment of the
cerebral vascular reserve capacity, and the fol-
low-up of patients with cerebrovascular diseases.
Doppler sonography provides a noninvasive but
accurate and repeatable means of measuring
CBFV in normal and pathologic subjects. The
main disadvantages of this method are its inabil-
ity to properly evaluate patients with highly set-
tled carotid bifurcation, coiling or kinking of
enlarged arteries, or calcified plaques. On the
other hand, it is a noninvasive, repeatable, and
affordable technique that can even be used for
bedside procedures. Our results, obtained in a
large and homogeneous adult population, offer
potentially useful reference data regarding total
CBFV, flow velocity, waveform parameters, and
cross-sectional area of the ICA and VA, with addi-
tional information regarding their sex differences
and age-related changes.
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