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952

Ultrasonic Measurement of the Elastic Modulus


of the Common Carotid Artery
The Atherosclerosis Risk in Communities (ARIC) Study
Ward A. Riley, PhD; Ralph W. Barnes, PhD;
Gregory W. Evans, MS; and Gregory L. Burke, MD, MS

Background and Purpose: The Atherosclerosis Risk in Communities Study is a prospective investigation
of the etiology and natural history of atherosclerosis and the etiology of clinical disease in four US
communities.
Methods: Noninvasive ultrasonic methods were used to determine mean wall thickness (WT), radius
(R), and circumferential arterial strain (CAS) in the left common carotid artery of 3,321 white male and
female study participants between the ages of 45 and 64 years. The mean and standard deviation of
Young's elastic modulus (Y) in 5 -year age groups were determined for each sex by combining the
ultrasonic data with concurrent noninvasive measurements of pulse pressure (PP) in the right brachial
artery using the equation Y=(R/WT)x(PP/CAS).
Results: Significant (/;=0.0001) age group differences in Y were observed in both sexes, with the mean
value increasing from 701 kPa in women and 771 kPa in men in the 45-49-year-old age group to 965 and
983 kPa, respectively, in the 60-64-year-old age group. Significant (p=0.0001) age group differences were
also observed for WT, the WT/R ratio, PP, CAS, and the PP/CAS ratio in both sexes. A sex difference in
Y was detected (male > female, p=0.0006) only in the 45-49-year-old age group. Significant (p< 0.0001)
sex differences were found, with men having a greater lumen diameter calculated as 2x (R-WT), a greater
WT, and a greater 2R in all age groups. The WT/R ratio did not differ in both sexes in all age groups.
Conclusions: Knowledge of the arterial wall elastic modulus and the parameters required for its
determination can provide important insight into structural changes occurring within the arterial wall
with age and sex, and possibly with the onset of very early arterial disease. (Stroke 1992;23:952-956)
KEY WORDS • carotid artery • risk factors • ultrasonics

T he concept of a longitudinal elastic modulus,


commonly referred to as Young's modulus (Y),
was introduced during the first decade of the
19th century to describe the aggregate elastic charac-
teristics of arterial wall constituents and structure.1
arterial strain (fractional diameter change) (CAS) oc-
curring during the cardiac cycle.3-4 By combining these
measures with noninvasive indirect estimates of arterial
blood pressure within the examined segments, Y can be
calculated. Y differs from other parameters used to
Before 1960, nearly all measurements of the elastic define arterial stiffness (e.g., compliance and distensi-
moduli of human arteries were performed on excised bility) in that WT is required for its determination.
tissue samples, providing results that one would expect Atherosclerosis is a disease of the artery wall, and a
to differ significantly from in situ values due to the knowledge of Y in a general population sample of
geometric, environmental, and structural changes asso- predominantly normal individuals can provide an im-
ciated with the vessel after excision.2 With the recent
portant reference for understanding arterial wall
development of noninvasive ultrasonic pulse-echo
changes that may occur before and during the early
methods, it became possible to directly determine with
high precision two important ratios required to obtain in stages of the disease. Consequently, Y may be an
vivo values of Y associated with the circumferential important parameter for characterizing the arterial wall
stretching of the artery wall: the ratio of arterial wall to study possible links between arterial wall composition
thickness (WT) to radius (R) and the circumferential and structure and cardiovascular disease risk, as well as
for monitoring changes in internal composition and
structure during studies of atherosclerosis progression
From the Departments of Neurology (W.A.R., R.W.B.) and and regression.5
Public Health Sciences (W.A.R., G.W.E., G.L.B.), Bowman Gray
School of Medicine, and AUTREC, Inc. (R.W.B.), Winston- The primary objective of this paper is to describe the
Salem, N.C. variation with age and sex, two major cardiovascular
Supported by National Institutes of Health contract N01- disease risk factors, of the mean value of Y in the left
HC- 55018. common carotid artery in 3,321 white adults between
Address for reprints: Ward A. Riley, PhD, Department of
Neurology, Bowman Gray School of Medicine, Medical Center the ages of 45 and 64 years who are participants in the
Boulevard, Winston-Salem, NC 27157-1078. ongoing Atherosclerosis Risk in Communities (ARIC)
Received February 7, 1992; accepted March 5, 1992. Study.6 Future reports will describe results in black

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Riley et al Elastic Modulus of Carotid Artery 953

participants and associations of Y with other established TABLE 1. Blood Pressure in Right Brachial Artery of Partici-
risk factors and prevalent cardiovascular disease. pants in Atherosclerosis Risk in Communities Study
Age N Diastolic Systolic
Subjects and Methods group
The ARIC Study is a prospective investigation of the (yr) F M F M F M
etiology and natural history of atherosclerosis and the 45-49 571 419 66.9±8.1 74.5±7.8 111.8±14.5 120.1±13.2
etiology of clinical disease in four US communities and 50-54 490 383 68.7±8.8 75.9±7.4 117.8±18.2 122.5 + 14.5
has been described in detail elsewhere.6 The ARIC
55-59 410 352 66.8±8.8 75.4±7.8 118.5±17.8 124.8±15.5
Study also measures variation in cardiovascular risk
factors, medical care, and disease by race, sex, place, 60-64 348 348 67.4±8.7 75.3±8.6 124.0±18.0 128.7+17.9
and time. A probability sample of residents aged 45-64 Values are mean±SD mm Hg. F, female; M, male. For diastolic
years is drawn from each community to take part in an blood pressure females<males in all age groups (p<0.0001); for
extensive evaluation of cardiovascular risk factors and systolic blood pressure females < males in all age groups
their sequelae. A major component of the evaluation is
an ultrasonic examination of the carotid arteries in
which ultrasonic pulse-echo techniques are used to (SBP) in the right brachial artery. The number of
measure arterial wall intima plus media thickness and subjects in each age/sex group ranged from 348 to 571.
the continuous variation of arterial diameter through- DBP remained constant with age in both sexes and was
out the cardiac cycle. Resting supine blood pressure is significantly (p<0.0001) higher in men than in women,
also measured in the right brachial artery at 5-minute by about 8 mm Hg. SBP was significantly (/?<0.0001)
intervals during the examination. higher in the older age groups in each sex, with SBP of
For a given material Y is defined as the ratio of stress men significantly (/><0.001) higher than that of women
(force per unit area) to strain (fractional change in in all age groups. In the oldest age group, SBP of men
linear dimension produced along the direction of the was about 5 mm Hg higher than that of women.
stress). For the case of an arterial segment that approx- Table 2 gives systolic lumen diameter (LD) of the left
imates a homogeneous thin-walled circular cylinder, Y common carotid artery by 5-year age/sex group. A
is denned as (R/WT) x (PP/CAS), where R is the arte- standard measure for quantifying atherosclerosis from
rial radius, WT is the arterial wall thickness, PP is the angiography, LD can be determined ultrasonically by
pulse pressure within the arterial segment, and CAS is measuring WT and 2R and computing the quantity
the fractional increase in arterial diameter during the 2 x ( R - W T ) . LD was significantly (/?<0.0001) larger in
cardiac cycle.2 The four dimensional parameters in this men than in women in all age groups, by about 0.60 mm.
equation are measured from an ultrasonic examination Within each sex, LD remained nearly constant with age,
of a longitudinal section of the left common carotid increasing very slightly in women.
artery in a 1-cm segment extending from 1 to 2 cm Table 2 also summarizes data for systolic WT. WT
proximal to the tip of the flow divider using standard- was significantly (p<0.0001) greater in men than in
ized ultrasound protocols as part of the ARIC Study.6-8 women in all age groups, by about 0.06 mm. Age groups
The presence of large, irregular, lumen-encroaching differed at p< 0.0001 in both sexes, increasing by about
lesions at this site is infrequent in this probability 0.12 mm from the youngest to the oldest age group.
sample, and identical standard protocols were used on Table 3 summarizes data for 2R. This value was
all subjects. significantly (/?<0.0001) greater in men than in women
R is one half of the arterial diameter associated with in all age groups, by about 0.80 mm, and increased in
the nearly circular cylindrical surface denned by the both sexes, by 0.50 mm in women and 0.30 mm in men
media-adventitia boundary. WT is the combined thick- from the youngest to the oldest age group. Data for the
ness of the intima plus the media.3 Both R and WT were WT/R ratio are also given in Table 3. No sex difference
measured on ultrasonic B-mode images. PP was mea- existed in any age group, but age groups differed at
sured in the right brachial artery with the subject at rest /?<0.0001 in both sexes. The WT/R ratio increased by
in the supine position. CAS was obtained using echo- about 0.02 from the youngest to the oldest age group.
tracking techniques to permit the arterial diameter to be
measured continuously during the cardiac cycle.4 This
model assumes that the contribution of the adventitia to TABLE 2. Systolic Lumen Diameter and Wall Thickness of Par-
the overall elastic properties of the artery wall is ticipants in Atherosclerosis Risk in Communities Study
negligible. Age Lumen diameter Wall thickness
Standard statistical analyses were performed on data group
obtained from 3,321 participants. Individuals who had (yr) F M F M
missing values for one or more variables required for 45-49 5.86±0.58 6.60±0.65 0.553±0.118 0.617±0.136
computing Y were excluded from the analysis. Mean 50-54 5.95+0.60 6.55±0.65 0.581±0.129 0.652±0.149
values are reported for each parameter by sex and the 55-59 5.95±0.60 6.61±0.72 0.638±0.149 0.700+0.179
5-year age groups 45-49, 50-54, 55-59, and 60-64
60-64 6.11 ±0.62 6.67±0.75 0.674+0.146 0.735±0.193
years. Age group and sex differences, and possible
interactions, were assessed using PROC GLM of SAS.9 Values are mean±SD mm. F, female; M, male. For lumen
diameter females<males in all age groups (p<0.0001). Small
Results age-sex interaction exists; in females age is associated with lumen
diameter (/><0.0001, 45-49<50-54=55-59<60-64), but in
Table 1 gives the number of subjects in each age/sex males it is not (p=0.1522, 45-49=55-59=60-64>50-54). For
group and the noninvasively determined resting dia- wall thickness females<males in all age groups (/xO.0001). Age
stolic blood pressure (DBP) and systolic blood pressure groups differ atp<0.0001 in both sexes.

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954 Stroke Vol 23, No 7 July 1992

TABLE 3. Average Arterial Diameter and Ratio of Wall Thick- TABLE 5. Pressure-Strain Elastic Modulus and Young's
ness to Radius of Participants in Atherosclerosis Elastic Modulus of Participants in Atherosclerosis Risk
Risk in Communities Study in Communities Study
Age Diameter (mm) Ratio Age Pressure-strain Young's
group group
(yr) F M F M (yr) F M F M
45-49 6.96±0.61 7.84±0.68 0.159±0.032 0.158±0.033 45-49 105 ±39 116±39 701 ±324 771±309
50-54 7.11 ±0.63 7.86±0.69 0.164±0.034 0.166+0.036 50-54 127±52 127±49 825±387 817±375
55-59 7.22+0.64 8.01 ±0.76 0.177±0.038 0.175±0.041 55-59 142±55 144±61 868±409 882±448
60-64 7.46±0.66 8.14±0.75 0.181 ±0.037 0.181 ±0.046 60-64 163 ±65 165±79 965±491 983±557
Values are mean±SD. F, female; M, male. For diameter Values are mean+SD kPa. F, female; M, male. For pressure-
females<males in all age groups (p<0.0001). Small age-sex inter- strain elastic modulus females<males only in 45-49 years age
action exists; in females age groups differ atp<0.01, and in males group (p<0.0001); age groups differ at/><0.0001 in both sexes.
means increase slightly but significantly (/)<0.05) between succes- For Young's elastic modulus female-cmale only in 45-49 years age
sive age groups, except 45-49=50-54. For ratio age groups differ group (p=0.0006); age groups differ at/?<0.0001 in both sexes.
at/?<0.0001 in both sexes; no age-sex interaction exists (/?=0.61).
sive ultrasonic B-mode imaging methods to measure
Table 4 summarizes data for brachial PP. PP was WT in the common carotid artery.10-16 Other studies in
significantly (p<0.0131) greater in women than in men humans and animals have used standard methods to
in all but the youngest age group, with the difference measure PP and noninvasive ultrasonic pulse-echo
between sexes being 3.2 mm in the oldest age group. tracking methods to measure CAS and consequently the
Age groups differed at /xO.0001 in both sexes. PP PP/CAS ratio.417-21 We report, from concurrent mea-
increased by 11.6 mm Hg in women and 7.7 mm Hg in surements of all four parameters, the first large popu-
men from the youngest to the oldest age group. Data for lation-based, multicenter, in vivo determination of Y in
CAS are also summarized in Table 4. A significant the adult human common carotid artery.
(/xO.0001) sex difference existed for CAS only in the The substantial increase in Y observed with age in
youngest age group, with values in women higher than both sexes implies a real change in the internal compo-
those in men, by 0.004. In the other three age groups sition and/or structure of the arterial wall. This increase
differences were of borderline significance in the same in Y was accompanied by a significant increase in WT.
direction. Age groups differed at /?<0.0001 in both However, arterial diameter increased slightly and ap-
sexes. CAS decreased by 0.010 in women and 0.009 in peared to compensate for the increase in WT to main-
men from the youngest to the oldest age group. tain a nearly constant LD. Over the same age range,
Table 5 summarizes data for both pressure-strain CAS decreased even though PP causing the artery to
elastic modulus (PP/CAS) and Y. A significant expand increased. As a result, PP/CAS also increased
(/><0.0006) sex difference existed for both PP/CAS and rapidly with age, at a rate greater than that for Y. Both
Y only in the youngest age group, with values in men elastic moduli increased significantly with age in each
higher than those in women, by about 10% for both sex.
variables. Age groups differed at p< 0.0001 in both sexes
However, a significant sex difference in Y was ob-
for both elastic moduli. PP/CAS increased by 58 kPa
served only in the youngest age group. Similarly, only in
(55%) in women and 49 kPa (42%) in men from the
the youngest age group was there a significant sex
youngest to the oldest age group. Y increased by 264
difference in PP/CAS. While an increase in Y with age
kPa (38%) in women and 212 kPa (27%) in men from
is to be expected, the absence of a sex difference in
the youngest to the oldest age group.
persons above 50 years of age is surprising. This is
Discussion particularly so if one considers that above 50 years of
age there was either a highly significant or borderline
Noninvasive determination of Y in the common ca-
significant sex difference in each term in the equation
rotid artery requires knowledge of the parameters R,
defining Y (i.e., WT, R, PP, and CAS). In addition,
WT, PP, and CAS. Various studies have used noninva-
DBP and SBP were consistently higher in men than in
women. However, values for the first of the two ratios
TABLE 4. Brachial Pulse Pressure and Carotid Artery Strain of (R/WT) in the defining equation were almost identical
Participants in Atherosclerosis Risk in Communities Study
for the two sexes in each age group, and values for the
Pulse pressure (mm Hg) Strain second ratio (PP/CAS) demonstrated no difference
group between the sexes above age 50 years. The absence of a
F M F M significant sex difference in these ratios in a general
(yr)
45-49 44.9±10.9 45.6±8.9 0.060±0.016 0.056±0.018 population sample of white men and women over 50
50-54 49.1±13.4 46.5 ±10.6 0.055±0.016 0.053±0.017 years of age is a very interesting observation arising
55-59 51.7+13.9 49.4±11.3 0.051 ±0.015 0.049±0.015 from this study.
60-64 56.5 ±14.6 53.3 ±13.3 0.050±0.016 0.047±0.016 That the pressure-strain elastic modulus tends to be
greater in men than in women below the age of 50 years
Values are mean±SD. F, female; M, male. For pulse pressure is confirmed by previous observations in two younger
females>males in all age groups (/X0.0131) except 45-49 years populations. At a mean age of 16 years, PP/CAS was 67
(p=0.3); age groups differ at/><0.0001 in both sexes. For strain
females>males only in 45-49 years age group (p<0.0001); in kPa in males and 62 kPa in females.4 A similar differ-
other age groups sex differences are marginally significant. Age ence of about 5 kPa was also observed in young subjects
groups differ at p<0.0001 in both sexes. with a mean age of 13.5 years.17 The lower values of

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Riley et al Elastic Modulus of Carotid Artery 955

both Y and PP/CAS in women aged 45-49 years in our measurements of PP/CAS have ranged from approxi-
study are consistent with these earlier observations if mately 10 to 20 kPa in younger and older subjects.417
the WT/R ratio in young subjects is also similar in the This is typically <15% of the mean value of PP/CAS
two sexes. This could suggest a change in arterial wall observed in a 55-year-old subject and is approximately
composition or structure related to menopause that one third of the increase in the mean value observed in
raises values in women to those in men. this population from the youngest to the oldest age
The relative constancy of the WT/R ratio in the two group. A detailed analysis of quality control data on a
sexes, whose arteries demonstrate substantial differ- subset of the ARIC Study population that will precisely
ences in the absolute values of WT and R, tends to estimate within- and between-observer variability re-
confirm the concept that this ratio evolves within an lated to these parameters is currently in progress.
arterial segment to satisfy a complex combination of These multiple observations on the ARIC Study
physical requirements related to optimal functioning of population demonstrate that a variety of potentially
the arterial wall.22"24 In spite of the fact that WT and 2R important physical changes occur in arterial dimensions
are markedly larger in men, the similarity of the WT/R and wall stiffness within a general population sample
ratio in men and women suggests that it may be a more while LD remains unaffected. A better understanding of
meaningful parameter than WT for attempting to de- the mechanisms producing these changes and how they
scribe relevant early atherosclerotic changes in arteries. might be modified could lead to new insights into the
The increase in the WT/R ratio with age may indi- very early stages of atherosclerotic disease.
cate, within the population sample, an increasing
amount of early arterial disease at this site. However, Acknowledgments
measurements of LD suggest no such increase. In fact, The authors wish to express their gratitude for the contri-
a careful look at the data suggests that there is a slight butions made to this study by the following individuals: Project
tendency for LD to increase, rather than decrease, with Office—Donna J. Neal and Patricia A. Smith; Forsyth County
age. This observation stresses the importance of relying Field Center—Amy Haire and Bonnie Monger; Jackson,
on measurements of the arterial wall (and diameter) Miss., Field Center—Alfredo H. Figueroa, Jane G. Johnson,
rather than LD in attempting to monitor the early stages Robert Smith, and Jessie M. Spencer; Minneapolis Field
of atherosclerosis. Center—Kenneth Cram, Bryna Lester, Gail Murton, and
As discussed in a previous article,4 blood pressure Kathy Provinzino; Washington County Field Center—Carol
measured in the brachial artery may not always accu- Christman, Dorrie Costa, Joel Hill, and Wendi McNulty; and
Ultrasound Reading Center—S. Omega Smith and Delilah
rately reflect blood pressure in the common carotid Cook.
artery. However, comparisons of intra-arterial pressure
in the large vessels with brachial artery pressures deter- References
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Ultrasonic measurement of the elastic modulus of the common carotid artery. The
Atherosclerosis Risk in Communities (ARIC) Study.
W A Riley, R W Barnes, G W Evans and G L Burke

Stroke. 1992;23:952-956
doi: 10.1161/01.STR.23.7.952
Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 1992 American Heart Association, Inc. All rights reserved.
Print ISSN: 0039-2499. Online ISSN: 1524-4628

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