© 1999 American Heart Association, Inc.
Atherosclerosis and Lipoproteins |
In the Femoral Artery Bifurcation, Differences in Mean Wall Shear Stress Within Subjects Are Associated With Different Intima-Media Thicknesses
From the Departments of Physiology (L.K., J.L., R.S.R.) and Biophysics (A.P.G.H.), Cardiovascular Research Institute Maastricht, Maastricht University, Maastricht, The Netherlands.
Correspondence to L. Kornet, PhD, Department of Physiology, Cardiovascular Research Institute Maastricht, Maastricht University, PO Box 616, 6200 MD Maastricht, the Netherlands. E-mail L.Kornet{at}FYS.Unimaas.nl
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Abstract |
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Abstract—In elastic arteries, intima-media thickening is more pronounced in areas with low than with high mean and peak wall shear stress. These findings in elastic arteries are not necessarily representative of the situation in muscular arteries. The former arteries have to store volume energy, whereas the latter are mainly conductive vessels. It was the aim of the present study to investigate noninvasively whether differences in wall shear stress within a muscular artery bifurcation, if any, were associated with different intima-media thicknesses (IMTs). The effect of age on the possible differences was assessed as well. We determined IMT and mean, peak systolic, and the maximum cyclic change in shear stress near the posterior wall in the common (FC) and the superficial (FS) femoral artery 20 to 30 mm from the flow divider in 54 presumed healthy subjects between 21 and 74 years of age. Results were considered in terms of intrasubject differences. Before the study, the reliability of the ultrasonic system to assess wall shear rate and IMT was determined in terms of intrasubject variability. IMT at the posterior wall was significantly larger in the FC than in the FS, probably owing to the significantly lower mean wall shear stress at this site in the FC. The relative differences in IMT and mean wall shear stress between FC and FS were independent of age. The difference in wall shear stress between both arteries can likely be explained by a different influence of reflections. In both the FC and FS, mean, peak systolic, and maximum cyclic change in shear stress near the posterior wall did not change significantly with age, whereas IMT did increase significantly with age.
Key Words: blood flow • intima-media thickness • femoral artery bifurcation • ultrasound • wall shear stress
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Introduction |
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Blood flowing through a vascular segment exerts a tangentially directed shear stress on the luminal surface of endothelial cells. Wall shear stress is the product of wall shear rate, ie, the radial derivative of the velocity near the wall, and local blood viscosity. Wall shear stress has been shown to be an important determinant for the release of vasoactive compounds from endothelial cells.1 2 3 4 5 Several vasoactive molecules stimulate the expression of adhesion molecules and chemokines involved in intima-media thickening.6 In studies relating flow measurements in scale models of human arteries and intimal thickening in corresponding series of autopsy specimens, it has been shown that in such arteries as the aorta,7 coronary arteries,8 and carotid arteries,9 10 11 the intima is thicker in areas with low than with high wall shear stress. Recently developed noninvasive ultrasound techniques have made it possible to study the relation between intima-media thickness (IMT) and wall shear rate and, hence, wall shear stress directly in humans. We showed in the common carotid artery of presumed healthy volunteers that the intima-media complex is thicker near the bifurcation than it is farther upstream, where wall shear stress is lower.12 The relative differences were found to be independent of age. These findings in mainly elastic arteries are not necessarily representative of the situation in purely muscular arteries because of the differences in function and structure between elastic and muscular arteries. Elastic arteries have to store volume energy, whereas muscular arteries are mainly conductive vessels.
Therefore, we investigated whether 2 sites in the muscular femoral artery bifurcation, ie, the common and the superficial femoral artery, are also subjected to different wall shear stresses and whether these differences, if any, result in different IMTs. Because it is yet unknown whether mean or peak systolic wall shear stress or the maximum cyclic change in wall shear stress during the cardiac cycle influences IMT, all 3 parameters were considered. We determined IMT and shear stress near the posterior wall in the common and the superficial femoral artery 20 to 30 mm from the flow divider. Measurements were performed on 54 presumed healthy subjects of varying age. Before this study, the reliability of the ultrasonic system to assess IMT and wall shear rate near the posterior wall in muscular leg arteries was determined in terms of intrasubject variability.
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Methods |
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Subject Population
Fifty-nine volunteers were invited to participate in the study. Five subjects were excluded because of a blood pressure >140/90 mm Hg3 or the presence of plaques in the common and/or the superficial femoral artery.2 These exclusions resulted in 54 volunteers who participated in the study. None of the volunteers used drugs known to modify hemodynamic parameters or had a history of cardiac, cerebrovascular, or peripheral vascular disease. The subjects were nondiabetic and nonhypercholesterolemic, and 11 were smokers. They refrained from smoking at least 1 hour before the measurements to avoid acute effects of smoking, if any, on the parameters to be measured. In 6 cases it was not possible to obtain the correct angle of insonation in the common femoral artery, and measurements were therefore performed in the superficial femoral artery only (the Table
). In 6 obese volunteers, the
superficial femoral artery was too deep (up to 100 mm) to be
visualized, and thus, only the common femoral artery was investigated
(the Table). Thus, 48 common and 48 superficial arteries were
used for further analysis. The study population had the
following age and sex distribution: 20 to 29 years (5 females, 2
physically active; 6 males, 4 physically active), 30 to 39 years (6
females, 2 physically active; 3 males, 2 physically active), 40 to 49
(6 females, 5 physically active; 4 males, 3 physically active), 50 to
59 (9 females, 5 physically active; 3 males, 2 physically active), and
60 to 74 years (8 females, 1 physically active; 4 males, 1 physically
active). A person was considered to be physically active if he or she
had a physically active profession or was involved in athletic
activities for >1 hour per week. From all volunteers, informed consent
was obtained before they entered the study. The study was approved by
the joint medical ethics committee of the Academic Hospital Maastricht
and the Maastricht University.
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Parameters to Characterize the Behavior of
Blood
The time-dependent wall shear stress near the posterior wall
(WSSp) exerted by flowing blood on the luminal
vessel wall can be derived from the wall shear rate
(WSRp) and the local whole-blood viscosity near
the posterior wall (WBVp) according to the
following equation:
WSSp=WSRpxWBVp,
where
WSRp=dv(r)/dr||r=R,
in which v(r) is the velocity distribution
assessed by means of ultrasound as a function of the radial position,
r is the local radial position, and R is the
radius of the artery. WSRp can be
determined directly by considering the velocity gradient close to the
posterior wall–lumen boundary. WBVp can be
estimated from plasma viscosity (
o) in
milli-Pascal–seconds and hematocrit (Ht) in percent; mean wall shear
rate near the posterior wall (MWSRp) in
second-1 can be determined by using the
approximation proposed by Weaver et al13 : log
WBVp=log o+(
xHt),
with =0.030(±0.005)-0.0076- (±0.0003) log
MWSRp. Because the plasma layer in a blood vessel
is only 3 to 7 µm,14 a factor that is 20 times
smaller than the spatial resolution of our wall shear rate–estimating
system, the effect of this layer on blood viscosity can be neglected,
and whole-blood viscosity only can be used for the determination of
wall shear stress. Plasma viscosity was determined by means of
capillary viscosimetry according to Wazer.15
Protocol
First, 2 venous blood samples were taken to determine hematocrit
and plasma viscosity to allow us to calculate blood viscosity (see
formula above). Next, data gathering started after an acclimatization
period of 10 to 15 minutes with the volunteers in the supine position.
The volunteer was connected to an ECG to generate a pulse that would
signal the onset of a cardiac cycle. With the use of the C9-5 ICT probe
(operating frequency of 5 to 9 MHz), the femoral artery bifurcation was
visualized and checked for the presence of plaques or stenoses.
Plaques were defined as a locally increased echodensity and/or
irregularity of the vessel wall. If plaques were present, the
volunteer was excluded from the study. If plaques were absent, we
checked with a linear probe whether the common femoral artery
was straight enough for 20 to 30 mm upstream from the bifurcation
to determine IMT at a well-defined angle of 90°. Furthermore, we
investigated whether the straight superficial femoral artery was not
situated too deeply to be visualized. The system was switched to
M-mode, and the IMT of the posterior wall was determined 8 times at 1
point in the common femoral artery 20 to 30 mm upstream from the
femoral artery bifurcation (location FC in Figure 1) and 8 times at 1 point in the
superficial femoral artery 20 to 30 mm downstream from the
bifurcation (location FS in Figure 1). The values averaged over
8 measurements were taken as the volunteers’ readings. Subsequently,
at both locations we determined the time-dependent velocity profile 18
times, and end-diastolic diameter was derived from the
diameter waveforms. The time-dependent velocity distribution was used
to calculate the time-dependent posterior wall shear rate. At each
location, mean, peak systolic, and maximum cyclic change in
posterior wall shear rate were derived from the posterior wall shear
rate waveforms. The values averaged over 18 measurements were taken as
the volunteers’ reading. Only the shear rates determined near the
posterior wall were used to study the relation between wall shear rate
and IMT because IMT can be reliable determined at the posterior wall
only owing to the large adventitia-intima boundary reflection at the
anterior wall, which prevents accurate assessment of the intima-media
boundary.16
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Assessment of IMT
The method used to assess IMT has been described in detail
before.16 In short, the common and superficial femoral
arteries were visualized in B-mode (ATL Mark 9, HDI, Advanced
Technology Laboratories). With the tip of the flow divider as a
landmark, the L 10-5 38-mm probe (operating frequency of 5 to 10 MHz)
position was manipulated until a suitable line of sight was obtained,
shown as a dashed line in Figure 1
. Along this line and starting
synchronously with a trigger derived from the peak of the R wave on the
ECG, radio frequency (RF) data were collected at a sample frequency of
20 MHz over a period of 4 seconds. After RF data acquisition, the first
line was displayed on a personal computer screen, allowing
identification of a 3-mm window covering the posterior lumen-wall and
interwall transitions. Data from this window over time were then stored
on hard disk for further offline processing. In this processing the
amplitude envelope of the RF signals was taken, and after phase
alignment of the signals, the time average of the envelope was
determined to reduce speckle interference. Subsequently, an
edge-detection algorithm was applied to the time-averaged envelope of
the processed RF signals. Like Wong et al,17 we found that
the media of the muscular superficial and the common femoral artery was
either echolucent or echogenic. Figure 2
shows the envelopes of the RF signals of a double- and a triple-layered
common femoral arterial wall as recorded in the same
subject at the same location. The position of the intima was assigned
to the point halfway along the first positive slope, where the
spatial derivative of the envelope first exceeded a preselected level
(threshold derivative was set at 0.020). The same procedure was
repeated for the next significant positive slope (system resolution was
set at 0.50 mm), which was required to reach a higher maximum than
the preceding positive slope (adventitia-intima amplitude ratio 
1).
In the upper panel of Figure 2, this is the second positive
slope and in the lower panel, the third positive slope. The difference
between the position of the intima and the media-adventitia transition
was defined as the IMT.
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Assessment of Wall Shear Rate and Diameter
The ultrasonic technique to estimate shear rate has been
described in detail elsewhere.18 19 The ultrasound echo
system (ATL Mark 9, HDI, Advanced Technology Laboratories) in
combination with dedicated signal processing is able to measure the
blood flow velocity distribution along a selected line of observation
across the center of the vessel. The superficial and common femoral
arteries were first visualized in B-mode by using the C9-5 ICT probe
(operating frequency of 5 to 9 MHz). Visualization of the posterior
wall of the superficial femoral artery was sometimes difficult because
the deep femoral artery was often situated at this site. After
positioning the M-line, shown schematically in Figure 1 as a
solid line, the ultrasound system was switched to echo M-mode with a
high pulse-repetition frequency and a short activation pulse.
Registration started synchronously with a trigger derived from the peak
of the R wave on the ECG. The captured RF signals (reflected and
scattered ultrasound signals) were digitized at 20 MHz and transferred
to the memory of the computer. Present memory capacity allows data
recording for 1.2 seconds, an interval normally sufficient for
capturing 1 complete heart beat. The first digitized RF line as a
function of depth was displayed on the computer screen. From the shape
and the position in depth of the reflections, the wall-lumen interfaces
on both sides were identified manually by placing sample volumes,
indicated by markers, on the reflections from the anterior and
posterior vessel walls. The distance between both markers, corrected
for the angle of observation (70o), was
considered as the initial (end-diastolic) inner diameter of
the common and the superficial femoral arteries. To obtain the
time-dependent blood flow velocity distribution, a modeled
cross-correlation function was employed to the RF data between the
markers to estimate the mean velocity over time segments of 10 ms
spaced at 5-ms (50% overlap) time intervals. The length of the RF
segments corresponded to 300 µm in depth, and the segments were
spaced at 150 µm intervals (50% overlap).18 19
Calculating the mean velocity for all RF segments resulted in a
time-dependent velocity profile, which was corrected for the angle of
observation (70o) (Figure 3, upper and lower panels). The shear
rate distribution was derived from the radial derivative of the
velocity profile at each site and at each time instant (Figure 3, middle panel). The maximum value of the derivative toward the
posterior wall of the vessel was considered as the estimate of the
instantaneous longitudinal posterior wall shear rate. From shear rate
distributions, mean wall shear rate near the posterior wall (in
second-1), which is the time-averaged shear
rate over 1 cardiac cycle, peak systolic wall shear rate near
the posterior wall (in second-1) and the
maximum cyclic change in wall shear rate within 1 cardiac cycle near
the posterior wall (in second-1) were also
determined.
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Variability
The absolute intersubject variability is the mean
variability between subjects. The intrasubject variability is the mean
variability within 1 subject. Because the common femoral artery could
not be examined in 6 cases and the superficial femoral artery could not
be examined in 6 cases, the intrasubject and intersubject variabilities
were studied on 48 common and 48 superficial femoral arteries.
Measurements within each subject were performed within 2 hours. The
variability for IMT and posterior wall shear rate for subject
i was determined by assessing the SD for that subject. The
mean variability for all subjects was corrected for the number of heart
beats in subject i (ni) and
calculated according to the following formula:
{[
nix(SDi2)]/ni}.
Statistics
Linear regression was employed to study the relation between 2
parameters. A significant relation was present if the
95% CI of the derivative excluded zero with a P
0.05. To
compare various age categories, we also used an ANOVA test. Multiple
regression was employed to study the relations between >2
parameters. Because both the common and superficial femoral
arteries could be examined in only 42 subjects, intrasubject
differences were analyzed in these subjects by using a paired
t test.
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Results |
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The absolute intersubject variations of IMT and of mean, peak, and maximum cyclic change in posterior wall shear stress for the various age groups as determined in both the common and superficial femoral arteries are presented in the Table
as mean values and
their SDs and reflect both measurement and biological variations. The
intrasubject variations reflect measurement variations only. The
intrasubject variation in IMT, as determined at the posterior wall in
the common and superficial femoral artery, was 11% and 8%,
respectively. In the case of averaging 8 repeated measurements, as in
the present study, the variation in averaged IMT will be 4% in the
common femoral artery and 3% in the superficial femoral artery. The
intrasubject variation in mean, peak, and maximum cyclic change in
posterior wall shear stress per measurement was 39%, 16%, and 17%,
respectively, in the common femoral artery and 25%, 16%, and 17%,
respectively, in the superficial femoral artery. In the case of
averaging over 18 measurements, as also performed in the present
study, the variation in averaged mean, peak, and maximum cyclic change
in wall shear stress will be 9%, 4%, and 4%, respectively, in the
common femoral artery and 6%, 4%, and 4%, respectively, in the
superficial femoral artery.
Within subjects, the IMT was significantly larger in the common than in
the superficial femoral artery (Figures 4 and 6). The relative difference in IMT between the common (FC)
and the superficial (FS) femoral artery
[(IMTFC-IMTFS]/[(IMTFC/2)+IMTFS/2)]x100)
amounted to 20% (95% CI of 14% to 25%, P=0.000; Figure 6) and was independent of age, sex, smoking, BMI, and physical
activity. A significant increase in IMT of the posterior wall with age
was shown in both arteries (Figure 4). Using multiple
regression, we found a significant influence of smoking and sex on IMT
in both arteries, , being larger in smokers and males, but not of BMI
and physical activity. In both arteries, no significant correlation
could be detected between IMT and diameter. The regression line through
the IMT-versus diameter (d) relation was as follows:
IMT=877+dx(-0.015) (SE=0.020, P=0.449, 95%
CI=-0.056 to 0.025) in the common femoral artery and
IMT=748+dx(-0.018) (SE=0.017, P=0.292, 95%
CI=-0.052 to 0.016) in the superficial femoral artery. The inner
end-diastolic diameter was 7.00±1.10 mm (mean±SD) in
the common femoral artery and 6.21±0.85 mm (mean±SD) in the
superficial femoral artery.
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Within subjects, mean posterior wall shear stress was
significantly lower in the common than in the superficial femoral
artery for all age groups (Figures 5A and 6). The relative difference in mean posterior wall shear stress
between the common (FC) and the superficial (FS) femoral artery
{[(MWSSP(FC)-MWSSP(FS))]/[(MWSSP(FC)/2)+(MWSSP(FS)/2)]100}
amounted to -38.1% (95% CI=-52.5% to -23.7%, P=0.000;
Figure 6) and was independent of age,
sex, smoking, BMI, and physical activity. No significant difference in
peak systolic and maximum change in wall shear stress was found
between the common and the superficial femoral arteries (Figures 5B, 5C, and 6). In both the common and the superficial
femoral artery, no significant correlation was found, with the use of
both tests, between mean, peak systolic, and maximum cyclic
change in wall shear stress on the 1 hand and age on the other (Figures 5A through 5C). By multiple regression in both the common and
the superficial femoral artery, a significantly larger mean wall shear
stress in males than in females and a significant positive correlation
between mean wall shear stress and BMI was found. Sex and BMI did not
affect peak systolic or maximal cyclic change in wall shear
stress. No influence of smoking or physical activity on mean, peak
systolic, and maximal cyclic change in wall shear stress could
be detected in these arteries. In both arteries, no significant
correlation between mean wall shear stress and diameter could be
detected. In the common femoral artery (FC),
MWSSp=0.412+(dx0.000) (SE=0.000,
P=0.728, 95% CI=0.000 to 0.000) and in the superficial
femoral artery (FS),
MWSSp=0.730+(dx0.000) (SE=0.000,
P=0.371, 95% CI=0.000 0.000). Also in both arteries, no
significant correlation was found between whole-blood viscosity and
diameter on the hand and age on the other.
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Discussion |
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The findings in this in vivo study show that within subjects, IMT is larger at the posterior wall in the common than in the superficial femoral artery, which may be explained by the lower mean wall shear stress at this site in the former.
In the common femoral artery, IMT varied between 0.5 and 1.2 mm
for healthy volunteers between 21 and 74 years of age. The latter value
corresponds well to the value of 
1.3 mm for healthy volunteers
70±5 years of age that has been described in the
literature.20 The intraindividual difference in IMT cannot
be attributed to a larger diameter in the common than in the
superficial femoral artery because in both arteries, no significant
correlation was found between diameter and IMT. Although sex and
smoking have an influence on IMT, this did not confound the outcome of
our study because we compared the differences in IMT between the common
and the superficial femoral artery within each subject. Therefore, we
conclude that the larger IMT in the common femoral artery is due to its
lower mean wall shear stress. The larger IMT in areas with lower mean
wall shear stress is in agreement with the results obtained in other
studies.9 12 21 22 23
The lower mean wall shear stress near the posterior wall in the common
than in the superficial femoral artery might be explained by a
difference in the effect of reflections at these 2 locations. Although
the maximum cyclic change in wall shear stress was not significantly
different between the common and superficial femoral artery, negative
flow occurs earlier in the cardiac cycle and lasts longer in the common
than in the superficial femoral artery (Figure 3). This can be
explained by the different perfusion areas of superficial versus deep
femoral arteries. In the superficial femoral artery, the reflections
are late, arising from a site situated far downstream that has a high
resistance at rest, whereas both early and late reflections occur in
the common femoral artery. The early reflections in the common femoral
artery originate from the deep femoral artery, also a site of high
resistance at rest. The longer duration of negative flow in the common
femoral artery explains why mean wall shear stress is lower in this
vessel.
Several explanations for the negative correlation between wall shear stress and wall thickness may be considered. First, the increased residence time of particles on the luminal surface of endothelial cells might lead to diffusion of particles into the wall, resulting in a larger wall thickness. Platelets and macrophages, key elements of atherosclerotic lesions, are more likely to adhere to the arterial wall in regions of increased residence time,24 especially because adhesion molecules are expressed in areas of low wall shear stress.6 Second, wall shear stress causes endothelial cells to become aligned in the prevailing direction of flow.25 26 27 Regions of enhanced shear stress are characterized by more elongated endothelial cells, whereas regions of relatively low shear stress are associated with more rounded endothelial cells.28 In the latter regions, cell turnover rates are higher than in the former.29 During cell turnover, intercellular junctions become leaky, allowing for an enhanced influx of lipids and other macromolecules. Therefore, the entrance into the wall of macromolecules, as lipids, may be enhanced in low-shear regions.30 Furthermore, wall shear stress has been shown to be an important determinant of the release from endothelial cells of vasoactive molecules,2 3 4 30 31 32 compounds that may stimulate the expression of chemokines involved in intima-media thickness.6
It should be noted that the maximum first derivative of the velocity
profile was considered and not the actual wall shear
rate.18 Shear rate at the wall cannot be determined owing
to the low scanning resolution relative to the arterial
diameter.19 Because the shear rate system is
activated with a short pulse and because spatial resolution,
determined by the length of the data window, matches system resolution,
the resultant resolution along the ultrasound beam is 0.3 mm.
Spatial resolution is hardly affected by the ultrasound beam width
(1 mm) because of the steep observation angle
(70o), but this makes measurement more sensitive
to minor deviations in observation angle. To overcome the problem of
low scanning resolution, the spatial maximum in shear rate was
considered as wall shear rate. Near the posterior wall, we may assume
the maximum shear rate to be 0.3 mm from the blood-intima
boundary. This implies that measured shear rate may underestimate wall
shear rate when the actual velocity gradient at the wall is steeper.
Therefore, shear rate as presented may be considered to be a
least estimate, because theoretically it is unlikely that the velocity
gradient will be less steep closer to the wall.
In this study, we used an intracavitary probe that, compared with a linear array, has the advantage that geometric broadening is small owing to a smaller aperture. Therefore, at a given angle, measurements are more accurate than with a linear probe. A disadvantage of the intracavitary probe is its handling, contributing to the relatively large variations in measurement.
The intrasubject variation in IMT assessment was 3% larger for
measurements performed in the superficial femoral artery (8%) than in
the common carotid artery (5%).19 This may be explained
by the fact that the deep femoral artery is situated at the proximal
site of the superficial femoral artery, making visualization of the
posterior wall of the superficial femoral artery more difficult than
that of the common carotid artery. The larger variability in assessment
of IMT in the common than the superficial femoral artery may be due to
the difference in geometry; ie, the common femoral artery was generally
slightly curved, whereas the segment of superficial femoral artery
investigated was usually straight. Therefore, errors in the angle of
observation (70° for shear rate and 90° for IMT measurements) were
more likely to occur in the common than in the superficial femoral
artery. Because an average of 18 shear rate measurements was used in
this study, the actual variation in mean wall shear rate will be 6%
in the superficial and 9% in the common femoral artery.
In conclusion, IMT at the posterior wall is larger in the common than in the superficial femoral artery, probably due to the lower mean wall shear stress at this site in the former. The difference in wall shear stress between both arteries can likely be explained by a different influence of reflections, being present during a longer part of the diastolic phase in the common femoral artery.
Received November 2, 1998; accepted March 24, 1999.
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