Arteriosclerosis, Thrombosis, and Vascular Biology. 1996;16:172-177
(Arteriosclerosis, Thrombosis, and Vascular Biology. 1996;16:172-177.)
© 1996 American Heart Association, Inc.
Blood Velocity Profiles in the Human Renal Artery by Doppler Ultrasound and Their Relationship to Atherosclerosis
Tokunori Yamamoto;
Yasuo Ogasawara;
Akihiro Kimura;
Hiroyoshi Tanaka;
Osamu Hiramatsu;
Katsuhiko Tsujioka;
M. John Lever;
Kim H. Parker;
Christopher J.H. Jones;
Colin G. Caro;
Fumihiko Kajiya
From the Departments of Medical Engineering, Systems Cardiology, and
Urology, Kawasaki Medical School, Kurashiki, Okayama, Japan (T.Y., Y.O., A.K.,
H.T., O.H., K.T., F.K.); the Centre for Biological and Medical Systems,
Imperial College, London, UK (M.J.L., K.H.P., C.G.C.); and the Princess of
Wales Hospital, Bridgend, UK (C.J.H.J.).
Correspondence to Tokunori Yamamoto, MD, Departments of Medical
Engineering and Urology, Kawasaki Medical School, 577 Matsushima, Kurashiki,
Okayama 701-01, Japan.
 |
Abstract
|
|---|
Abstract Blood velocity profiles were measured in the renal
branch
(diameter 5.9±1.3 mm) of the aortorenal bifurcation using
a
20-MHz 80-channel pulsed Doppler velocimeter during
retroperitoneal
surgery in 10 patients. The peak Reynolds number was
1145±140
and the frequency parameter (Wormersley
parameter) was 3.0±0.8.
Immediately distal to the ostium
of the renal artery, reverse
flow, indicating flow separation, was
observed near the cranial
wall mainly during the first part of the
cardiac cycle. There
were flows from the cranial to the caudal side of
the artery
at this location, indicating the presence of strong
secondary
flows. Two diameters downstream of the ostium, the velocity
profiles
were skewed to the caudal side in all patients. Four diameters
downstream,
the flow profile was symmetrical (3 patients) or only
slightly
skewed (7 patients) and virtually parabolic throughout the
cardiac
cycle. These observations mean that the flow on the cranial
side
of the renal branch of the human aortorenal bifurcation is
characterized
by (1) a bidirectional oscillation of the
flow, (2) separation
of the flow during systole, and (3) low
time-averaged shear
rate. These blood velocity patterns may be
related to the localization
and development of
atheromatous plaque that occurs preferentially
in this
region of the renal artery. Conversely, the unidirectional,
axisymmetrical
flow found in more distal parts of the renal artery are
associated
with a very low incidence of lesions.
Key Words: atherogenesis • aortorenal bifurcation • low time-averaged shear rate • flow separation • flow oscillation
|
Introduction
|
|---|
In the renal artery of
humans, atherosclerotic plaque occurs
primarily in the region 1 to 2 cm
downstream from the renal
ostium.
1 2 3
When plaque occurs
and develops sufficiently to
disturb renal blood flow and reduce renal
perfusion pressure,
renal hypertension can occur, making plaque
development in this
region very important clinically. According to the
response-to-injury
hypothesis for
atherosclerosis, many different risk factors
can lead
to endothelial dysfunction,
4 and a large
number of
growth factors, cytokines, and vasoregulatory
molecules may
participate in its development.
5
It is widely recognized that hemodynamic factors play
an important role in vascular biology and in the localization and
development of atherosclerotic lesions. Despite its importance, the
characteristics of blood flow near the renal ostium have been studied
only in model tube flows6 7 and by a computer
simulation.8 Recently, advances in Doppler ultrasound
techniques have enabled us to measure velocity profiles in vessels up
to 
7 mm in diameter.9 10 11 Using a
high-frequency,
range-gated Doppler ultrasound device, we have measured the
velocity profiles at various sites around the aortorenal bifurcation in
dogs.12 Dogs, however, do not develop
atherosclerosis spontaneously, although
atheromatous lesions can be produced by diets with very
high lipid levels or by hypothyroidism.13
The high susceptibility of the ostial region of the renal artery in
humans1 2 3 and the very low
susceptibilities of more distal
regions provide the opportunity for assessing which
hemodynamic features are associated with lesion
development. In particular, distinctions can be drawn between the
effects of reversing and nonreversing blood flow close to the vessel
wall. To characterize the flow patterns, we have used
high-resolution multigated Doppler ultrasound to measure the
instantaneous velocity profiles throughout the cardiac cycle at three
different locations near the ostium. Because of the complexity of the
local hemodynamics at the bifurcation, it was necessary
to make measurements at different beam angles to the axis of the renal
artery to determine the different components of the velocity
vectors.
|
Methods
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We studied a total of 10 patients (7 men, 3 women) who were
admitted
to the Department of Urology, Kawasaki Medical School (see
Table
1
). Their clinical diagnoses were renal cancer (4
men, 3 women),
retroperitoneal lymph node metastases of testicular
cancer (2
men), and neuroblastoma (1 man). None of the patients had
abnormal
renal function tests,
hypercholesterolemia, or thoracic or abdominal
arterial
calcification. The geometry of the aortorenal
bifurcation was
examined by DSA, CT, and/or MRI. In none of the
patients was
an atherosclerotic change in the aortorenal bifurcation
region
discernible.
The investigations were approved by the Medical Ethics Committee of the
Kawasaki Medical School, and informed written consent was obtained from
all of the patients studied. During the abdominal surgery, none of the
patients had bleeding for which blood transfusion was required. Radical
nephrectomy, enucleation of tumor, or retroperitoneal lymph node
dissection was performed under modified
neuroleptoanesthesia (with pentazocine and diazepam)
because of its minimal influence on renal flows.14 This
anesthesia was induced by thiopental (4 mg/kg) followed by
succinylcholine chloride (1 mg/kg). After tracheal intubation,
pancuronium (4 mg), pentazocine (30 mg), and diazepam (10 mg) were
administered. The lungs were ventilated mechanically with a mixture of
nitrous oxide and oxygen (FIO2=0.3). Operation postures
were supine position (3 patients) or left or right side up (7
patients). The angle of the operating table for the side-up
position was 30° to 40° from a horizontal plane. The angle of the
aortorenal bifurcation was assessed from the DSA, CT, and MRI scans,
and the blood velocities were obtained before nephrectomy, enucleation,
or dissection. The intraoperative velocity measurements were
accomplished within 10 minutes without any disturbance of the
operative procedure. The blood pressure was measured in the left renal
artery, and the electrocardiogram was monitored in lead
II.
Blood velocity profiles were measured with a high-frequency
(20 MHz) pulsed Doppler velocimeter, which
was developed in the Department of Medical Engineering, Kawasaki
Medical School, in collaboration with Fujitsu Lab Co and has been
described previously with detailed validation of the velocity patterns
it measures.9 10 11 In brief, this device
measures the
Doppler shift from 80 channels with sample volumes with a radius of
0.5 mm and a thickness of 0.2 mm. Being extravascular, the
measuring probe does not influence the intravascular blood flow. The
Doppler signals are analyzed simultaneously by
a zero-cross method and by FFT. The high-pass filter had a
cutoff frequency of 375 Hz, which corresponds to a velocity of 1.5 cm
s-1 with a probe angle of 60° to the vessel axis.
In all the patients, the velocity profiles were measured at four sites
in the renal artery, as indicated in Fig 1. For
comparison of results in different patients, all measurements were made
relative to D measured in each patient just downstream from the ostium
from the DSA, CT, or MRI scans. Site 1 was 0.5 D, site 2 was 2 D, and
site 3 was 4 D distal to the ostium, where the artery was somewhat
narrower. Measurements were made at all three sites with the probe
placed on the cranial side of the vessel at an angle of 60° to the
axis of the vessel. We called the main forward flow component in the
first part of the cardiac cycle the systolic flow wave and the
smaller flow component in the latter part the diastolic
flow wave (see Figs 2, 3, and 4),
although there was
some time delay from cardiac systole and diastole due to
pressure wave propagation. To determine the direction of the velocity
in the more complex flows that were observed at site 1, measurements
were also made with the probe at 90° to the vessel axis (site 1P).
The exposed vessels were bathed in ultrasound gel, and the probe was
held at the required angle with a probe holder. The lateral position of
the probe was adjusted until the velocity profiles were of maximum
width, indicating that the ultrasound beam was traversing the midline
of the vessel. Care was taken not to alter the geometry of the vessels
being measured.
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Figure 1. Sketch of the aortorenal bifurcation showing the
Doppler ultrasound measurement sites. The angle between the
ultrasound beam and renal artery axis was 60° for sites 1, 2, and 3
and 90° for site 1P. D indicates diameter of the proximal portion of
the renal artery.
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Figure 3. A typical example of the blood velocity profiles
measured during a cardiac cycle at site 2 (see Fig
1 ).
|
|
Two hydrodynamic parameters that characterize the flow are
the Reynolds number (Re) and frequency parameter (
),
which can be calculated as follows:
 | (1) |
 | (2) |
where D is the diameter of the vessel, Up the peak
velocity, 
the frequency of the cardiac cycle, and 
the density
and µ the coefficient of the viscosity of blood. These
parameters were calculated for each patient, the Reynolds
number being calculated for peak velocity measured at site 2. This was
in the single channel displaying the maximum velocity. The Reynolds
number based on the peak velocity rather than the more common mean
velocity is quoted because it provides an upper bound for these highly
pulsatile flows and is therefore more useful in assessing the
probability of turbulent flows during the whole of the cardiac
cycle.
|
Results
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Bifurcation Geometry and Hemodynamic
Parameters
The proximal portion of the renal artery lies more ventral
than
the
abdominal aorta and then passes to the most dorsal surface of
the
abdominal cavity. The diameter of the abdominal aorta, measured
just
upstream of the aortorenal junction, ranged from 18 to
24 mm. The
diameter of the renal artery, measured half a diameter
distal to the
ostium, ranged from 3.0 to 7.0 mm. The angle between
the aorta and the
renal artery ranged from 60° to 90°.
In the whole patient group,
the mean blood pressure was 96±10
mm Hg, the mean peak Reynolds number
was 1145±140, and
the mean frequency parameter was
3.0±0.8. Turbulent flows
are unlikely to be found at these Reynolds
numbers and frequency
parameters.
15 All of the
results for the geometry and hemodynamic
parameters
are given in Table 2
.
Blood Velocity Profiles
Fig 2 shows the
velocity profiles measured in one patient at site
1, immediately distal to the orifice of the renal artery. Site 1 refers
to measurements taken with the probe at 60° to the vessel. The upper
panel is the velocity as a function of time, determined from the FFT of
the Doppler signal. The lower panel shows velocity profiles across
the vessel, calculated by the zero-cross method measured at
20-millisecond intervals during the portion of the waveform indicated
by the vertical lines. The inbuilt algorithm used by the ultrasound
device to compute the velocities is based on the assumption that the
velocity vectors are parallel to the direction of the vessel's axis.
We have attempted to overcome this problem by using the technique of
vector addition of signals obtained with the probe oriented at
different angles to the vessel axis. The FFT velocity waveform was
obtained from the channel containing the maximum velocity (as assessed
by the zero-cross method) at each measuring time. The velocity
waveforms indicate that there is continuous forward flow throughout the
cardiac cycle. The velocity profiles showed that in all the patients,
reverse velocities were present at the cranial side of the vessel
during the period of systolic flow wave and also during the
period of diastolic flow wave, but the duration of reverse
flow in a cardiac cycle at the cranial side wall was variable. The
maximum reverse/forward velocity ratio, defined as the ratio of the
maximum value of reverse velocities across the vessel in a cardiac
cycle to the maximum value of forward velocities, for 10 patients was
0.3±0.1. In most of the period of the diastolic wave, flow
was maintained in the forward direction, though velocities were below
threshold close to both walls.
The velocity vector measured at site 1P
with the probe perpendicular to
the vessel had a component directed from the cranial to the caudal side
of the vessel, particularly during the period of the systolic
flow wave, indicating the presence of secondary flow. An example is
shown in the upper left panel of Fig 5. This flow
component toward the caudal direction occurred between the cranial wall
and the point within the vessel where the peak velocity was measured at
site 1. It became smaller and reversed near the caudal wall. Vector
addition of the velocities measured at site 1 (V1) and site
1P (V1P) gives the two-dimensional velocity vector (V)
in the medial plane of the vessel at this site (upper right panel of
Fig 5). The technique for vector addition and the assumptions
made have
been previously described.12 These vectors, calculated at
the beginning of the systolic wave, at the time of peak forward
flow, and in the early and late diastolic waves (A, B, C,
and D in Fig 5), are shown in the bottom panel of Fig
5. A rotation of
the flow, typical of separated flows, is apparent, and the velocities
are skewed, mostly toward the caudal wall.
The velocity waveform and
velocity profiles measured at site 2, 2 D
downstream of the bifurcation, are shown in Fig 3. The velocity
is
still greatest on the caudal side of the vessel in all patients, but
the reversed flow near the cranial side wall seen at site 1 was not
detectable with our cutoff frequency. The results measured at site 3, 4
D downstream of the bifurcation, are shown in Fig 4. The
velocity
profiles are much more axisymmetrical; a slight skewing toward the
caudal side was apparent during the period of peak systolic
flow wave in seven patients, but the other three patients showed a
completely symmetrical pattern. Two of seven patients with skewed
velocity profiles at site 3 were in the supine position and the other
five patients were side up. One of three patients with symmetrical
profiles was supine and the other two were side up. Accordingly, the
patient's position did not seem to affect the results, although the
number of data was limited. There was no noticeable difference in the
velocity profiles at site 3 among the seven patients with renal cancer
(two symmetrical and five slightly skewed) and the three without (one
symmetrical and two slightly skewed).
|
Discussion
|
|---|
Early atherosclerotic lesions tend to be found at bifurcations
and
curving regions of arteries, and it has been suggested that
hemodynamic
factors play an important role in their
development. The current
study was undertaken to investigate this
problem by measuring
the blood velocity profiles, with high spatial
resolution, of
the renal arteries of humans during retroperitoneal
surgery.
The measurements were necessarily performed on a group of
surgical
patients with renal abnormalities. Those with discernible
atherosclerosis
were excluded. The similarity of the
velocity profiles in patients
presenting with markedly different
clinical conditions suggested
that these particular abnormalities were
not important in modifying
the hemodynamics. The major
findings of this study are that
the velocity pattern near the cranial
wall at the renal ostium,
at which atherosclerotic lesions are prone to
develop, is characterized
by (1) separation of the flow mainly in
systole, with velocity
vectors directed toward the caudal wall and (2)
a time-varying
oscillation of flow. Both of these
conditions will give rise
to a low time-averaged shear rate at this
site.
There are many reports on the occurrence of
atherosclerosis in the renal artery, although the
frequency of occurrence of lesions in this vessel appears to be much
less than in the aorta or coronary arteries.16 17
Most reports lack precision about the location of the lesions within
the vessel, but DeBakey et al18 found that in patients
requiring operation for atherosclerotic obstruction of the renal
artery, 74% of the lesions were localized at a proximal site close to
the renal ostium. Yutani et al3 found that in vessels from
subjects who had hypercholesterolemia, intimal
thickening and foam cell infiltration were more prominent in the
proximal wall than in the more distal wall in a variety of ostia,
including that of the renal artery. More recently, Nguyen and
Haque19 carried out a survey of lesion distribution in the
abdominal aorta and its major branches in 18 human autopsy specimens.
The autopsy specimens were chosen by the absence of diffuse
atherosclerotic involvement, which might mask the focal distribution of
the disease, and the number of lesions in each of 35 different segments
throughout this region was reported. Plaques were found on the cranial
wall of the renal artery, within one diameter of the ostium, in 14 of
18 specimens on the left side and in 12 of 18 on the right side. The
incidence of lesions at these locations was among the highest of all
the 35 sites studied. On the caudal wall of the renal artery, within
one diameter of the ostium, the incidences were 7 of 18 and 8 of 18 on
the left and right sides, respectively. In keeping with earlier reports
on the paucity of renal artery lesions, this study showed plaques
further downstream in the vessels in only 1 of 18 cases on the left
side and 1 of 18 on the right side.
The variation in velocity patterns close to the vessel wall found in
this study may be related to these pathological observations. The site
at which lesions have been most commonly observed, the cranial wall of
the proximal regions, is that which showed a transient region of flow
separation in all 10 patients. In the early part of the cycle,
velocities close to the wall, and therefore the local wall shear
stresses, were in the reverse direction, while in the remainder of the
cycle, velocity and shear stress were in the forward direction. At the
caudal wall of the proximal region, where lesions occur less
frequently, there were strong secondary flows in all patients,
indicating that the shear stress would have a circumferential component
and then change in both magnitude and direction during a cardiac cycle.
In the distal part of the vessel, the most notable feature was the
axisymmetry and unidirectionality of the profiles throughout the cycle.
In pathological studies, this region has been found to be remarkably
free from atherosclerotic lesions. The velocity patterns at this distal
site are in marked contrast to the reversing patterns of flow seen in
various parts of the aorta and particularly in the epicardial
coronary arteries, sites where the prevalence of lesions is
very much greater. The local dependence of lesion development and the
presence of variation in direction of shear found in the renal artery
appear similar to that found in the carotid sinus.20
From this study, it would appear that blood flow separation, with its
attendant reversing shear stress, may be a strong correlate of
atherogenesis, lesions being more prevalent at sites where there is
flow separation than at those with unidirectional flow. We have not
attempted to quantitate the wall shear stresses applied to the wall
from the velocity profiles, because even with the very high resolution
of our technique, there is still uncertainty about the position of the
vessel wall, which moves during the cardiac cycle. Inspection of the
velocity profiles, however, indicates that shear rates close to the
wall and hence shear stresses are likely to be higher on the caudal
wall of the proximal region of the renal artery than at more distal
sites. The lower incidence of atherosclerosis in the
more distal regions suggests that low shear without flow reversal may
be associated with fewer lesions, while higher shear stresses may not
be completely protective.
Previous authors have drawn attention to the potential importance of
branching angle.21 Nguyen and Haque19 tried
to correlate the distribution of lesions in the different specimens to
the branching angle between the renal arteries and the abdominal aorta.
They found a weak inverse correlation between the angle and the
incidence in the part of the aortic wall between the renal artery and
the aortoiliac bifurcation but did not draw attention to any
correlation between that angle and incidence of lesions in the renal
artery itself. Our patients exhibited a range of angles between 60°
and 90°, but this did not appear to alter the main features of the
velocity profiles. These features were also retained in an earlier
series of experiments on dogs when the aortorenal angle was actively
changed between 90° and 30°.12 The angle of the
aortorenal bifurcation is altered by respiratory movements of the
diaphragm, by changes in posture, and during movement, but our results
would suggest that these factors would not markedly alter the local
shear forces.
Concluding Remarks
These studies on human patients shed
further light on the
relationship between hemodynamic factors and
atherosclerosis. Since the lesions within the renal
artery appear to be highly localized, it is possible to demonstrate
that flow separation, which causes a transient reversal of wall shear
stresses, appears to be the most important causative factor, while
unidirectional flow appears protective. It has been suggested that the
stagnation of blood, which is associated with regions of flow
separation, may be an important factor in this
association.2 22 23 Our study shows,
however, that the
separation zone persists only for about one third of the cardiac cycle,
so that the residence time of blood components close to the wall is
relatively short. Even in regions with no flow separation or reversal,
such as in the more distal regions of the renal artery, where lesions
are rarely found, the velocity profiles suggest that there may be
stagnation of blood close to the vessel wall during the latter part of
the cycle because of the very low axial velocity.
|
Selected Abbreviations and Acronyms
|
|---|
| CT |
= |
computed
tomography |
| D |
= |
diameter of the proximal
portion of the renal artery |
| DSA |
= |
digital
subtraction angiography |
| FFT |
= |
fast Fourier
transform |
| MRI |
= |
magnetic resonance
imaging |
|
|
Acknowledgments
|
|---|
This research was supported by grant-in-aid 05454278 for
General
Scientific Research (B) and 06671366 (C) from the Ministry of
Education,
Science and Culture, Japan. We thank Chikako Tokuda and
Mieko
Hayashi for their assistance in manuscript preparation.
Received June 15, 1995;
accepted October 16, 1995.
|
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Top
Abstract
Introduction
