Am J Physiol Heart Circ Physiol 285: H384-H391, 2003.
First published March 13, 2003; doi:10.1152/ajpheart.00729.2002
0363-6135/03 $5.00
Assessment of spatial inhomogeneities in intima media thickness along an arterial segment using its dynamic behavior
Jan M. Meinders,1
Lilian Kornet,2 and
Arnold P. G. Hoeks1
Departments of 1Biophysics and
2Physiology, Cardiovascular Research Institute
Maastricht, University Maastricht, 6200 MD Maastricht, The Netherlands
Submitted 20 August 2002
; accepted in final form 5 March 2003
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ABSTRACT
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To assess locally deviating structural and mechanical properties of
arterial walls, the spatial variance in end-diastolic intima media thickness
(IMT) and the change in IMT during the cardiac cycle (
IMT) were
determined along a short segment of the common carotid artery (15.86 mm), at
16 positions simultaneously. Intrasubject spatial inhomogeneities along the
artery were revealed by a spatial variance significantly larger than the
temporal variance over several beats. If differences between positions were
confirmed, the extent of the inhomogeneity was obtained by comparison of IMT
and IMT at each position with their spatial medians ± the
least-significant difference. Because no intersubject comparisons were
necessary, a single session of several measurements was sufficient to assess
inhomogeneities in the arterial wall properties of a subject, making the
method independent of biological variability between subjects. The method was
evaluated on 47 presumed healthy subjects (age range 21–75 yr). In 22
subjects, spatial inhomogeneities in IMT occurred (P <
0.05). In young subjects, IMT was locally decreased, i.e., in systole
inhomogeneities were less compressed than their surrounding tissue. In older
subjects, IMT was locally increased, i.e., the inhomogeneity was
locally more compressed than its surrounding wall tissue.
ultrasound; radial strain; compressibility; arterial stiffness
IN THE EARLY DEVELOPMENT of cardiovascular disease (CVD),
arteries first become more elastic, whereafter they stiffen
(11,
20). Assessing these locally
changed structural and mechanical properties noninvasively in a single subject
is difficult mainly due to the small spatial and temporal changes involved.
Even at more advanced stages, changes in arterial wall properties are hard to
determine because most methods suffer from low sensitivity and specificity.
For instance, even though an increased intima media thickness (IMT) of the
common carotid artery (CCA) marks changing vessel wall properties and seems to
be a potential candidate to predict the future development of CVD
(15,
21), the correlation between
increased carotid IMT and CVD is weak. This weak correlation is a result of
CVD being a focal phenomenon confined to the intima with a relatively small
thickness (
2.5% of IMT). Only in more diseased arteries does the intima
constitute >20% of the IMT. The correlation between IMT and CVD is further
attenuated due to the physiological effects of aging
(16). Hence, carotid IMT has
to be significantly increased (1.2 mm) to be conclusive
(1). To enhance sensitivity,
IMT is analyzed along an arterial segment and several measurements are
averaged (3). However, recent
lesions, fatty streaks, more advanced lesions (atheroma), and fully developed
complicated plaques tend to be localized at specific sites
(2), resulting in only a
locally deviating IMT, which is obscured by averaging over relatively long
arterial segments.
The low specificity and sensitivity of methods in determining arterial wall
properties usually originate from large intersubject variations and low
precision of the employed method in relation to the stage of the disease. To
get a more specific and sensitive indicator, either multiple properties have
to be determined simultaneously
(9) or one property has to be
determined several times separated either in space or time. The ankle arm
pressure index is an example of a simultaneously assessed property separated
in space (23). The advantage
of this method is that random physiological fluctuations, e.g., in pressure,
are canceled. However, a unique cutoff to ascertain CVD is difficult to
define, mainly due to the large spatial separation of measurement sites and
biological variability between subjects
(12,
22). Endothelial dysfunction
of superficial arteries is an example of a temporally separated determined
property at a specific position. It can be assessed by a comparison of
endothelium-dependent changes in diameter due to ischemic occlusion and
endothelium-independent dilatation due to administration of sublingual
glyceryl trinitrate (7).
However, also in this case, a clear cutoff value for CVD is not available,
again mainly due to biological variability between subjects
(14).
It can be anticipated that early changes in the structural properties of
the arterial wall are revealed by the IMT and especially the change in IMT
during the cardiac cycle (IMT). Moreover, spatial heterogeneity in the
structural properties of the arterial wall is expressed by the spatial
variance in IMT and IMT. Additionally, the extent of the spatial
variance in IMT or IMT over a short arterial segment reveals whether
the change in elasticity is a local phenomenon at the site of the developing
lesion (spatial inhomogeneity) or involves the total arterial tree
(18). To avoid definition of a
global cutoff value, sensitive to intersubject variations, the temporal
variance in IMT or IMT at one position is used as an estimate for the
assessment precision, i.e., a cutoff value above which the spatial variance
indicates possible inhomogeneities.
It was the aim of this study to determine whether local inhomogeneities can
be assessed by comparison of simultaneously obtained spatial and temporal
variances. Therefore, IMT and IMT were assessed over a short arterial
segment at 16 positions covering 15.8 mm. The spatial variance over multiple
positions was compared with the temporal variance over several beats using
ANOVA. If heterogeneity was confirmed, the extent of the lesion
(inhomogeneity) was obtained by comparing the deviating IMT and IMT
with their medians ± the least significant difference (LSD). The
proposed method was evaluated on 47 presumed healthy subjects.
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MATERIALS AND METHODS
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IMT waveform measurement. With the use of a 7.5-MHz linear array
transducer and fast B-mode, the wall movement of an artery segment of 15.86 mm
was assessed at 16 adjacent positions simultaneously
(18). The spatial sample
distance of 1.06 mm matched the beam width in the focal point. Briefly, the
frame rate of an echo system (Pie Medical 350; Maastricht, The Netherlands)
was increased to 651 Hz by increasing the pulse repetition frequency from
6,944 to 10,416 Hz, by increasing the interspacing between individual B-mode
lines with a factor 4 and by utilizing only 50% of the transducer length. With
the use of a specially developed data-acquisition system, the radio frequency
(RF) data of each line were stored in the memory of a personal computer. The
envelope of 16 RF lines was displayed on the screen of the ultrasound scanner,
providing a real-time B-mode image. Wall positions were determined for each R
wave top peak of the ECG. The high frame rate allowed cross-correlation of
subsequently recorded RF lines, resulting in high-precision wall tracking
(5,
6). The depth window size for
the correlation procedure was set to the resolution of the system, i.e., 0.3
mm, equivalent to eight sample points at a sampling frequency of 21.3 MHz. The
temporal window size was set to seven frames, converting to a temporal
resolution of 10 ms at a frame rate of 651 Hz
(18). Because the underlying
RF lines in a B-mode image are registered sequentially, a time skew between
registered distension waveforms exists. To compensate for this time skew,
images were made orthogonal with respect to time by linear interpolation
(17).
The change in diameter (d) as a function of time t at
position p [d(p,t)] was obtained by placing
tracking windows at the adventitia-media interface of the anterior wall and
the media-adventitia interface of the posterior wall
(Fig. 1A). The IMT
waveform [IMT(p,t)] was obtained by positioning the tracking windows
at the lumen-intima and media-adventitia interface of the posterior wall
(Fig. 1B). Because of
the passing pulse pressure, the diameter increases from a minimum to a
maximum, whereas IMT decreases from a maximum to a minimum. The maximum
diameter between two ECG triggers defines the peak-systolic diameter, whereas
the minimum in diameter between the ECG trigger and peak-systolic diameter
defines the end-diastolic diameter. The time points at which peak-systolic and
end-diastolic diameters are obtained also determine the peak-systolic and
end-diastolic IMT (dotted lines in Fig.
1). Subtraction of end-diastolic IMT from IMT(p,t)
results in the change in IMT during the cardiac cycle for each position
p [IMT(p,t); Fig.
1C]. As a result of our definitions, maximum diameter
changes have positive values, whereas IMT have negative values. The
above calculations were performed for each line separately.
Statistical analysis. A space- and time-dependent observation of
IMT or IMT, qpm, can be expressed as
 | (1) |
in which µ is the overall mean, 
pm is the random
error term (noise), 
p is the change in
qpm associated with position p (spatial
variation), and 
m is the change in
qpm associated with measurement m
(temporal variation). It was assumed that pm,
p, and m are normally
zero mean distributed and that no interaction between the different terms
exists. The random error term, pm, can be
interpreted as the precision of the system to determine IMT or IMT at
any time or position. The random error term is clearly visible in
Fig. 1 as the beat-to-beat
stepwise transition in IMT and IMT, which is caused by the
determination of the wall position for each beat
(Fig. 1). The variance in IMT
or IMT over time depends on pm +
m, whereas the variance in IMT or IMT over
space depends on pm + p.
In the absence of any spatial and temporal variations, both
p and m are zero. The
temporal variation, m, depends on beat-to-beat
physiological variations, e.g., the change in pressure due to breathing
(0.3 Hz) or the baroreflex (0.1 Hz), and is shown in
Fig. 1 as superimposed on the
stepwise transition. If the contribution of the temporal variation to the
temporal variance is small, the temporal variance can be used as an estimate
for pm. If a spatial inhomogeneity exists,
p increases and the ratio of spatial and temporal
variance is larger than unity. A significantly increased spatial-to-temporal
variance ratio can be used as an indication for inhomogeneities. The
computational procedure to obtain spatial and temporal variances and the test
for significance are explained below.
The temporal variance follows from the average of the variances over all
measurements at each position, that is
 | (2) |
in which 
p is the average
over all measurements at position p, nm is the
number of considered measurements, and np is the
number of positions along which the parameter is determined
(18). The spatial variance can
be obtained by determining the average of the variances over all positions
during each measurement, that is
 | (3) |
in which m is the average
over all positions during measurement m. Assuming normally zero-mean
distributed pm, p, and
m, and no interaction between the different terms,
the spatial variance can also be obtained from the variation in
p
 | (4) |
in which is the overall mean.
Equation 3 determines the mean of the variances, whereas Eq.
4 determines the variance of the mean.
The ratio of Eqs. 2 and 4 results in an F
distribution allowing the use of ANOVA to compare the spatial and temporal
variance (19). F
values were obtained according to
 | (5) |
F values larger than a critical F value indicate that one or
more positions are significantly different from the others, a clear indication
of a locally deviating arterial wall property. Critical F values can
be obtained from the F distribution with a significance level of 0.05
and np - 1 and
np(nm - 1) degrees
of freedom for the spatial and temporal variances, respectively. F
values and critical F values were obtained for each subject
individually.
In the above calculations, all positions are compared with each other,
i.e., it is determined whether minimum and maximum values differ significantly
from each other. To exclude those results with an accidentally large
difference between minimum and maximum, values must also be within the median
± the least significant difference (LSD). The LSD can be obtained from
 | (6) |
in which
tnp(nm
- 1)(0.05) is the Student's t-test value with
np(nm - 1) degrees
of freedom and a significance level of 0.05
(19). The LSD constraint
increases sensitivity.
Study subjects. Validation of the proposed method was performed
through an in vivo study in 47 (29 women and 18 men) presumed healthy
volunteers ranging in age from 21 to 75 yr (mean age 49 ± 13 yr). All
subjects gave written informed consent to participate in the study, which was
approved by the joint medical ethical committee of the Academic Hospital
Maastricht and the University Maastricht. The site of measurement was a
straight longitudinal section of the left CCA with the most distal RF line
2–3 cm proximal to the bifurcation and the scan plane perpendicular to
the plane of the bifurcation as established with the echo system. In each
subject, six independent measurements were made. The recording time of each
measurement was 6 s, covering at least five cardiac cycles (intersubject
average 6.4). An ECG was recorded simultaneously with the B-mode measurement.
The pulse pressure was determined in the left brachial artery using an
oscillometric blood pressure meter (Omron 705CP). IMT and IMT obtained
for all beats in one measurement were averaged, resulting in six measurements
consisting of end-diastolic IMT and IMT determined at 16 positions.
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RESULTS
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Figure 1 shows the diameter
(A), IMT (B), and IMT (C) waveforms as a
function of time for three cardiac cycles for a 36-yr-old male subject. The
thin solid lines are the waveforms for all 16 positions, whereas the thick
solid line is the average over all positions. End-diastolic and peak systolic
diameter are indicated by the vertical dotted lines (first beat only). These
lines also indicate the end-diastolic and peak-systolic IMT, respectively.
Intersubject end-diastolic diameter, distension, IMT, and IMT are
summarized in Table 1,
subdivided into male and female subjects and ages below and above 50 yr. The
temporal variation was visible as a transition in diameter and IMT at the
beginning of the second and third beat
(Fig. 1, A and
B). The distribution of the individual waveforms in
Fig. 1 shows the spatial
variance in diameter, IMT, and IMT. Median intrasubject spatial and
temporal SDs in end-diastolic diameter, distension, IMT, and IMT are
summarized in Table 2. The
median intrasubject temporal SD indicates the precision of the system to
assess IMT (80 µm) and IMT (30 µm).
The IMT increase per year for younger subjects (21–50 yr) was lower
than that for the older subjects (Fig.
2A). The spatial (open circles) and temporal (solid
circles) variances in IMT are displayed as a function of age in
Fig. 2B.
Figure 2C presents the
F values (open squares) and critical F values (solid line).
The number of positions (N) different from the median ± LSD is
depicted in Fig. 2D. A
negative value for N indicates a locally smaller IMT, whereas a
positive N indicates a locally larger IMT. Although statistics
indicated that there were several subjects with significantly different IMT
(i.e., F value > critical F value), there were only two
subjects with a difference larger than one LSD from the median, i.e.,
N <> 0. For these two subjects, the IMTs as a function of
position are displayed in Fig. 3,
A and B, respectively. The arrows indicate the
positions that are significantly different from the median IMT. Visual
inspection of the IMT for all other subjects revealed no inhomogeneities.
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Fig. 3. IMT as function of position for a 48-yr-old female subject with a
significantly decreased IMT (arrow in A) and a 52-yr-old male subject
with a significantly increased IMT at 2 positions (arrows in B). The
thin solid lines are single measurements. The thick solid line is the average
of all measurements (36 beats). The dashed line indicates the median
IMT.
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Figure 4A displays
IMT as a function of age. There was a tendency for IMT to become
larger beyond 50 yr. Figure
4B shows a larger spatial variance (open circles)
compared with the temporal variance (solid circles). The precision in
determining IMT was estimated at 30 µm (equal to the median temporal
SD; Table 2). The better
precision in determining IMT compared with IMT (80 µm) was a
result of the cross-correlation procedure between RF lines, which determines
the displacements of walls by estimation of the phase shift between two
successively recorded B-mode frames
(5,
6,
18). The larger spatial
variance was also expressed by the larger F values (open squares,
Fig. 4C) compared with
the critical F values (solid line,
Fig. 4C) and the
number of positions, N, that are significantly different from the
median IMT (Fig.
4D). Figure
5A shows a subject having at five positions (indicated by
the arrows) a significantly larger IMT, whereas
Fig. 5B shows a
subject having at two positions a significantly lower IMT.
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DISCUSSION
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To reveal spatial inhomogeneities in structural and mechanical properties
of an arterial wall, the spatial intrasubject variances in end-diastolic IMT
and IMT along the arterial segment were compared with the temporal
variance using ANOVA. Significantly increased spatial variance indicates
locally deviating structural and mechanical properties. The extent of these
spatial inhomogeneities in end-diastolic IMT and IMT can be obtained
from the number of positions significantly different from the median ±
LSD. Because the ratio of the spatial and temporal variances together with the
critical F value were assessed within a subject, the detection of
inhomogeneities was insensitive to biological variability between subjects.
Furthermore, only a small set of measurements (6) was required to approach
the precision of the system under physiological conditions (temporal
variance), because six measurements of 6 s reduces the effect of respiration
(0.3 Hz) and the baroreflex (0.1 Hz) effectively.
Usually a relatively high threshold is necessary to distinguish deviating
IMT from population means because of the combined effect of intersubject SD
(150 µm, SD in Table 1)
and the precision to assess IMT (80 µm, SD in
Table 2). Simultaneously
assessed IMT during several measurements at several closely spaced positions
allowed within-subject comparison of spatial and temporal variances. Increased
spatial variance indicates spatial heterogeneity, where it is assumed that the
temporal variance can be used as an estimate for the precision of the system
to obtain IMT. Increased temporal variation, e.g., due to physiological
variation in pressure as a result of breathing or the regulation of the
baroreflex during the measurements, increases the temporal variance (Eq.
2), which not only lowers F values (Eq. 5), but also
increases the LSD, thus lowering the probability to detect a spatial
inhomogeneity. This decreasing sensitivity ensures a low percentage of false
positive interpreted results (high specificity).
Despite possibly large temporal variations, the sensitivity of the method
was high, as illustrated by the relative large number of subjects having a
spatial variance higher than the temporal variance, i.e., large F
values compared with the critical F value
(Fig. 2C). In
comparing the spatial with the temporal variance using ANOVA, all positions
were compared with each other, i.e., if the minimum and maximum were
significantly different from each other, the F value became larger
than the critical F value. Restricting our results only to those
cases that differed significantly from the median, thus excluding accidental
large differences between minimum and maximum, revealed only two subjects with
an inhomogeneity in IMT (Fig.
2D). For the subject with a significantly smaller IMT at
one position, IMT decreased linearly as a function of position
(Fig. 3A). Important
to note is that the deviating IMT (383 µm) was only 97 µm smaller than
the median (480 µm), i.e., slightly exceeding the system precision (80
µm). For the other subject, the larger IMT (836 µm) compared with
the median (676 µm) at two positions
(Fig. 3B) was also
visible in the original B-mode image (white arrows in
Fig. 6).
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Fig. 6. B-mode image of a 62-yr-old male subject with significantly increased IMT
at 2 positions (see also Fig.
3B). The arrows indicate the site of the lesion. The
B-mode image consists of 16 lines and was displayed in real time on the
ultrasound scanner.
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Although IMT is not the same as elasticity, it can be envisaged that
it will change when artery wall properties are altered
(8,
10). Intrasubject comparison
of spatial with temporal variance in IMT showed inhomogeneities in a
surprisingly large number of subjects (Fig.
4D). At younger ages, these inhomogeneities were
predominantly positive (N > 0), whereas at older ages these
inhomogeneities were negative (N < 0). A positive inhomogeneity in
IMT indicates a locally less decreased IMT during the cardiac cycle,
i.e., the surrounding tissue is more compressed than the site of the lesion
itself. The example shown in Fig.
5A illustrates that IMT locally even increases during the
cardiac cycle (IMT > 0), suggesting possible displacement of wall
mass from adjacent parts of the arterial wall to the focal site
(8,
10). Other subjects with
positive inhomogeneities showed similar features. Whether this type of
inhomogeneity is correlated to a decrease in stiffness during early
development of atherosclerosis is not clear. The negative inhomogeneities at
older age showed the opposite effect, i.e., the inhomogeneity was more
compressed than the surrounding wall tissue (local IMT > median
IMT). Possibly the wall mass is displaced from the focal site to the
surrounding tissue or the elastic behavior of the artery is locally indeed
increased, e.g., due to an accumulation of proteoglycans in the arterial wall
(4).
It should be noted that the previous results do not necessarily mean that
the complete circumferential wall area is compressed or stretched, because the
wall material can be nonuniformly displaced around the arterial wall.
Intravascular ultrasound confirmed that at sites with focal lesions the radial
strain (equal to IMT/IMT) was decreased, whereas at other sites (in the
radial direction) strain was increased, thus preserving total circumferential
wall volume (10). Hence, it
may be concluded that for a noncircumferential focal lesion, the plane of
observation has a large influence on whether a significant compression or
stretch is obtained. To determine whether a lesion is circumferential and to
exclude erroneous results in determining compression of arterial walls,
ultrasound observations should be made at two orthogonal directions. It can be
envisaged that a noncircumferential inhomogeneity is compressed in one field
of view, whereas it will be stretched in the perpendicular field of view.
The surprising results for heterogeneity in IMT and IMT were
obtained with high accuracy. This high accuracy was a result of sequentially
applying two different statistical tests. The F test compares the
spatial with the temporal variance, implicitly testing the precision of the
system. That is, both spatial and temporal variances depend not only on the
spatial (p) and temporal
(m) variations but also on the precision
(pm, Eqs. 2 and 3). Decreased
precision results in lower F values (Eq. 5), thus lowering
sensitivity to reveal inhomogeneities. Significantly increased F
values only indicate that there are differences among the different positions.
In fact, we tested whether the extrema were significantly different from each
other with a confidence level of 95%. LSD compares each individual position
with the median, thus enhancing sensitivity to a confidence level of maximal
99.75%. Also, in this case, lower precision, i.e., increased temporal
variance, lowers sensitivity due to increased LSD values (Eq. 6).
Hence, a significantly different IMT or IMT indicates inhomogeneities
with a high confidence level.
Because the method as described above is independent of the echo line
density in the current spatial observation window, there seems to be no
objection in performing the same statistical analysis on B-mode images
recorded on video, which usually have a higher line density than the fast
B-mode system presented here. However, because complex cross-correlation of RF
signals is not possible on video data, the observed change in IMT during the
cardiac cycle will be less precise. The relative large temporal variance will
decrease sensitivity for determining heterogeneities in IMT
considerably. Hence, only more advanced techniques to determine IMT and
IMT allow detection of inhomogeneities in (video) B-mode images. An
advantage of video images is the larger spatial observation window, thus
increasing the possibility to detect a lesion. However, the sensitivity to
small lesions will decrease, due to the relatively smaller contribution of the
small lesion to the spatial variance.
In conclusion, intrasubject comparison of spatial and temporal variations
in IMT and IMT exposed locally deviating arterial wall properties.
Because no intersubject comparisons were necessary, a small set of
measurements was sufficient to assess inhomogeneities in the arterial wall
properties of a subject. Because of the high precision to determine
end-diastolic IMT, small spatial variations in IMT could be detected with a
high sensitivity. Sensitivity in determining spatial variations in IMT
was even higher because of the complex correlation method used to detect wall
motion. For young subjects, IMT was locally decreased, i.e., the
surrounding is more compressed than the site of the inhomogeneity. For older
subjects, IMT was locally increased, i.e., the inhomogeneity was
locally more compressed than its surrounding tissue.
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ACKNOWLEDGMENTS
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This work was supported by Grant BTS97126 from Senter, Ministry of Economic
Affairs, The Netherlands.
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FOOTNOTES
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Address for reprint requests and other correspondence: J. M. Meinders, Dept.
of Biophysics, CARIM, Univ. Maastricht, PO Box 616, 6200 MD Maastricht, The
Netherlands (E-mail:
j.meinders{at}bf.unimaas.nl).
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby marked
"advertisement" in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
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Copyright © 2003 by the American Physiological Society.
TOP
ABSTRACT
MATERIALS AND METHODS
), i.e., ratio
of spatial and temporal variation, are compared with the critical F
values (solid line) in C. The number of positions (N)
significantly different from the median IMT (
) are displayed in
D.
