From the Departments of Psychiatry (K.A.M., J.F.O.) and Surgery (S.K.W.),
University of Pittsburgh School of Medicine, and the Department of
Epidemiology, Graduate School of Public Health, University of Pittsburgh
(K.A.M., L.H.K., K.S.-T., H.C.L.), Pittsburgh, Pa.
Methods—The magnitude of change in blood pressure and heart rate
from rest to public speaking and mirror image tracing, two stressful
tasks, was measured. Average intima-media thickness (IMT) and focal
plaque in the common carotid artery, bulb, and internal carotid artery
were measured with the use of duplex ultrasonography on average 2.3
years later.
Results—The average IMT was 0.77 mm, with a range of 0.60 to
1.37; 52.5% had at least one plaque. Correlational analysis
showed that greater IMT was associated with greater pulse pressure
change during mental stress (r=0.17,
P<0.01). Statistical adjustments for possible
confounders (age, hormone replacement therapy use, resting pulse
pressure, smoking status, and triglyceride levels) did not
alter the results. The plaque index was associated with greater pulse
pressure change during the mirror image tracing task (odds ratio=1.47,
P=0.01) for women with a plaque score of
Conclusions—Mental stress–induced pulse pressure changes may
influence the development of early atherosclerosis in
the carotid artery of women. Widening of pulse pressure during stress,
as well as at rest, may be a marker of compromised compliance in the
vessel wall.
Atherosclerosis in the carotid arteries is a marker of
generalized atherosclerosis throughout the body,
including the coronary arteries.5 Carotid
arteries are an easily accessible site for B-mode ultrasound
measurement of IMT as well as focal plaque. IMT is thought to be an
early marker of diffuse
atherosclerosis6 7 8 but may also
represent thickening specifically due to elevated BP or both.
Standard risk factors for CHD, eg, age, SBP and DBP, LDL
cholesterol, history of CHD, smoking, and diabetes are
associated with IMT,9 10 11 even in healthy
postmenopausal women.12 13 Furthermore, several
population-based studies show that high levels of IMT in
asymptomatic men and women predict new clinical CHD and
stroke, even when investigators controlled statistically for major
cardiovascular risk
factors.14 15 16 Thus, ultrasound measures of
carotid IMT and plaque can provide a test of the association of the
cardiovascular risk associated with mental stress
responses.
To our knowledge, only two studies related to the mental stress
hypothesis used ultrasound measures of carotid
atherosclerosis. In one study,8 a
smaller change in HR during mental stress was associated with greater
carotid plaque in a sample composed of hospital outpatients with high
levels of risk factors or symptoms of vascular disease and community
volunteers. In a subsample of unmedicated participants, progression of
atherosclerosis was more substantial among those who
showed greater SBP responses to stress.8 A second
study showed that BP increases during mental stress were correlated
with mean IMT and plaque height among Finnish men aged 46 to 52 years
but not among older men.17 Subanalyses
showed that the association persisted among younger men when
investigators adjusted for standard CHD risk factors and among the
subgroup of 135 unmedicated younger men with no symptomatic
cardiovascular disease. The objective of the
present study was to test whether healthy middle-aged women who
exhibit large BP and HR increases during two mental stressors were at
high risk for the development for early carotid
atherosclerosis. The mental stress testing took place
on average 2.3 years before the ultrasound measures, and study
participants were free of medications that affected the
cardiovascular system at the time of mental stress
testing.
All women completed a baseline examination and then reported their
menstrual status monthly. When women reported that they had stopped
menstruating and/or had taken HRT for 12 months, they were considered
postmenopausal; they were reevaluated at that time and at 2, 5, and 8
years after menopause. Starting in September 1993, the carotid
ultrasound measures were added to the protocol for women who were
evaluated at 5 or 8 years after menopause.
Participants
Mental Stress Protocol
Subjects rested quietly for the first 10 minutes of the testing. During
this time the BP was measured three times—at 5, 7, and 9 minutes—to
establish an average of resting baseline BP. Maximal inflation for the
automatic BP cuff was then adjusted to a predetermined value, which was
After a second rest period of 10 minutes with BP recorded at 6 and
8 minutes, participants were given instructions to prepare a speech on
an assigned topic covering specific points. Participants were
instructed to pretend that they had been shopping and were examining a
wallet, when a plainclothes detective approached them and accused them
of shoplifting. Their task was to prepare a speech defending themselves
before a magistrate and include what they thought should happen to the
plainclothes detective. Participants had 2 minutes to mentally prepare
their speech, after which they delivered their speech for 3 minutes.
The speech was recorded, and BP was measured at 30 and 120 seconds.
The content of the speech was chosen because it worked successfully in
other studies conducted in our laboratory with middle-aged
women.20 The speech task elicits a strong
ß-adrenergic response and typically elicits the largest
cardiovascular response in our battery of mental stress
tasks.
Carotid Ultrasound Protocol
Trained readers measured the mean IMT across 1-cm segments of
the near and far walls of the distal common carotid artery and the far
wall of the carotid bulb and the internal carotid artery on both right
and left sides. Measures from each location were then averaged to
produce an overall measure of IMT; three women could not be scored for
mean IMT because of missing data from at least one site. A
computerized reading program developed for the
Cardiovascular Health Study11 and
modified in Pittsburgh was used. Readers also scored the ultrasound
images for plaque in the proximal common artery, distal common artery,
carotid bulb, internal carotid artery, and external carotid artery; one
woman lacked a plaque score. Plaque was defined as a distinct area of
hyperechogenicity and/or a focal protrusion into the lumen of the
vessel. For each segment, the degree of plaque was graded as follows:
0=no plaque; 1=one small plaque <30% of vessel diameter; 2=one medium
plaque between 30% and 50% of the vessel diameter or multiple small
plaques; 3=one large plaque >50% of the vessel diameter or multiple
plaques with at least one medium plaque. The grades were summed across
right and left carotid arteries to create an overall measure of extent
of focal plaque.
Reproducibility of IMT and the plaque index was assessed in five women
who underwent two ultrasound examinations within 1 week. Each time the
women were scanned by two separate sonographers, and each scan was
scored by two readers. When we accounted for both sonographer and
reader variation, the intraclass correlation was 0.86 for IMT and 0.96
for the plaque index.
Data Analysis
Because the distribution of IMT was skewed, the IMT data were first
transformed to yield a normal distribution. Then Pearson correlations
between IMT and the summed standardized residual stress scores were
calculated to evaluate the association of overall task reactivity and
carotid disease. IMT scores for individual sites were not
analyzed separately because of lower reproducibility of
individual sites than for mean values across sites. Because
mental stressors elicit different patterns of
hemodynamic responses, the overall stress
analysis was followed by correlational analyses for
each stressor separately with the use of residualized scores.
Then the associations were evaluated by multiple regression by
adjustment for age at the time of the ultrasound scan, use of HRT and
baseline BP or HR at stress testing, ever-smoking status, and
triglyceride levels at the time of the scan. Ever-smoking
status, triglycerides, and BP were included because a
separate report showed that these variables were the strongest
independent predictors of IMT and plaque in 200 of the women included
in the present analysis as well as in 292 of the 294 women
who were candidates for the present
analysis12 21 ; other risk factors, eg,
total cholesterol or HDL cholesterol, were
nonsignificant when the above variables were
included.12 To illustrate the significant
associations, women were categorized into four nearly equal groups
according to the distribution of IMT scores, and the unadjusted task
minus baseline mean values are presented.
Women were categorized into three groups: no plaque, plaque score of 1,
and plaque score of
Because of eligibility criteria to enter the study in 1983, the women
were relatively healthy in the present sample. In addition, the
sample for analysis excluded 40 women who were on medication at
the time of the mental stress testing because those medications would
affect the magnitude of the stress-induced BP or HR response. In
consequence, the remaining women described in this report can be
considered healthy, without known clinical disease. The mean IMT
of the sample was 0.77, with a range of 0.60 to 1.37. Approximately
half the women had at least one plaque, with 25% having a plaque index
of 1 and 27% having a plaque index of
The mean baseline BP and HR of the sample were in the normal range
(Table 2
Associations Between Stress-Induced Cardiovascular
Responses and Early Carotid Disease
Multiple regression analysis adjusted for potential confounders
showed that IMT was correlated with the pulse pressure during the
combined tasks (ß=0.18, P<0.006) and during the mirror
image tracing task (ß=0 .22, P<0.0006). In addition, IMT
was correlated with DBP during mirror image tracing (ß=-0.14,
P=0.03).
Plaque index was not related to the residual scores summed across tasks
but was associated with decreasing DBP residualized scores
(P<0.02) and increasing pulse pressure residualized scores
(P=0.02) during mirror image tracing (Figure 3
It is thought that stress-induced cardiovascular
responses lead to increased atherosclerosis because of
changes in shear stress and catecholamine release, which
damage the endothelium and allow the infiltration of
lipids and macrophages into the intima, leading to intimal
thickening and the development of fibrous plaque. However, given that
stress-induced SBP and HR change scores were not associated with
subsequent IMT or plaque index, it is more likely that other factors
played a role in this sample of relatively healthy, middle-aged
women.
Pulse pressure, which was associated with subsequent IMT and plaque
index during mirror image tracing, is determined approximately by the
ratio of stroke volume output to compliance of the arterial
tree, which is, in turn, affected by change in mean
arterial pressure and pathological changes affecting the
distensibility of the arterial
wall.22 As arterial walls age, they
lose much of their elasticity and muscular tissue, and sometimes these
are replaced by fibrous tissue and plaque that cannot
stretch.23 In consequence, compliance of the
arterial system is reduced, which causes the
arterial pressure to rise greatly during systole and to
fall greatly during diastole as the blood runs off from the
arteries to the veins. Furthermore, aging of the arteries, especially
in the presence of high BP, leads to abnormal response to
endothelium-dependent vasodilator, such as
acetylcholine.24 Individuals who exhibit frequent
increases in pulse pressure during stress may accelerate the rate of
aging in their arterial tree. On the other hand, it is also
possible that prevalence of diffuse disease or focal plaque may lead to
an increase in pulse pressure both during rest and during stress, even
after statistical adjustment for stress levels. We cannot discount this
possibility because carotid ultrasound measures were added to the study
protocol after the inclusion of mental stress measures. Future research
on progression of carotid disease will allow more definitive
conclusions about the direction of effect in healthy postmenopausal
women.
Although the findings from this study point to the importance of
stress-induced changes in pulse pressure for early carotid
atherosclerosis in women, they do not preclude the
importance of stress-induced increases in BP, cardiac output, or
catecholamine release in the early development of
atherosclerosis. The sample is unique, ie, middle-aged
women with low levels of risk factors and no frank clinical disease at
the time of stress testing. Perhaps in individuals with high levels of
risk factors or overt disease, as studied
elsewhere,8 17 these indicators of sympathetic
activation may be more critical. Stress-induced sympathetic responses
may be more important in men, who develop
atherosclerosis earlier than women. The associations
between pulse pressure and carotid disease were stronger for the mirror
image tracing task, a task validated to elicit a
vasoconstrictive response, than for the speech task, a
task validated to elicit a ß-adrenergic response. This could be
interpreted as suggesting that pulse pressure responses during stimuli
that normally elicit a vasoconstrictive response are
especially prognostic. Because the tasks were administered in fixed
order as a result of being embedded in a long, complex epidemiological
protocol, it is also possible that the effects were stronger for the
mirror image tracing task because that task was administered first and
was more stressful to the participants. Arguing against that
explanation is that the magnitude of change was smaller during the
mirror image tracing task than during the speech task. Nonetheless,
this study demonstrates the importance of stress-induced changes in
pulse pressure in predicting the development of early
atherosclerosis in the carotid artery. Widening of
pulse pressure during stress, as well as at rest, may be a marker of
compromised compliance in the vessel wall indicative of heightened risk
in women.
Received March 16, 1998;
revision received May 4, 1998;
accepted May 4, 1998.
© 1998 American Heart Association, Inc.
Original Contributions
Stress-Induced Pulse Pressure Change Predicts Women's Carotid Atherosclerosis
Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Background and Purpose—Individuals
who exhibit large increases in blood pressure and heart rate during
mental stress may be at risk for accelerated
atherosclerosis. This report evaluates the association
between stress-induced hemodynamic responses and
carotid atherosclerosis in 254 healthy
postmenopausal women. 
2 versus 1 or 0, adjusted for possible confounders.
Key Words: atherosclerosis • carotid arteries • risk factors • stress, psychological • women
Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Individuals vary
widely in the magnitude of their BP and HR response to mental stress.
The magnitude of the response appears to be reliable across repeated
assessments and does not simply reflect an emotional reaction, nor is
it correlated with the amount of chronic stress in an individual's
life. Individuals who exhibit frequent and large
cardiovascular responses might be prone to accelerated
coronary
atherosclerosis.1 In support of
this hypothesis are the results from several small studies showing that
coronary patients exhibit larger responses to mental stress
than do healthy control subjects, and male coronary patients
who are especially reactive to mental stress are more likely to have a
subsequent clinical event.2 Furthermore, a recent
prospective analysis showed that coronary patients in
whom myocardial ischemia can be induced by mental stress are at
higher risk of a coronary event during the subsequent several
years than their counterparts.3 The results from
animal research in which the cynomolgus monkey was used are
consistent with the proposed atherogenic effect of reactivity
to mental stress. Male and female animals that exhibit the largest HR
response to an experimenter approaching them with a monkey glove have
the greatest amount of histologically confirmed
coronary
atherosclerosis.4
Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Study Overview
From 1983 to 1984, 541 premenopausal women were enrolled in a
study of changes in biological and behavioral characteristics of women
as they experienced the menopause. They had been contacted by letter
sent to randomly selected women living within certain zip codes in
Allegheny County, Pennsylvania, and were subsequently interviewed by
telephone regarding the following eligibility criteria: age 42 to 50
years; menstrual bleeding within the last 3 months; no surgical
menopause; DBP <100 mm Hg; and no medications known to influence
biological risk factors under study, eg, lipid-lowering, insulin,
thyroid, estrogens, antihypertensive, and psychotropic medications.
Sixty percent of eligible women volunteered. The University of
Pittsburgh Institutional Review Board approved the project
protocol, and all participants gave informed consent for their
participation. Participant characteristics and recruitment procedures
are described in detail elsewhere.18
Starting in March 1991, women were administered the mental
stress protocol. Two hundred ninety-four women who completed mental
stress testing previously and who completed the fifth or eighth year
examination underwent the carotid ultrasound protocol as of March 1995.
An additional 98 women had mental stress testing but not carotid
ultrasound protocol at that point: 1 woman died; 5 declined
participation; 3 moved out of the area; and 89 women were ineligible
because they were not at least 5 years past the menopause. Of the 294,
40 women were taking medications known to influence the
cardiovascular system at the time of the mental stress
testing (eg, ß-blockers) and were excluded from analysis.
Embedded in the larger clinical evaluation was the mental stress
protocol. SBP, DBP, and HR were monitored with an IBS model SD-700A
automated BP monitor (Industrial and Biomedical Sensors Corp)
with a standard occluding cuff placed on the participant's nondominant
arm. It employs a low-frequency sensor mounted on the cuff to detect
arterial wall motion and Korotkoff vibrations. Detection of
Korotkoff vibrations, in addition to sounds, enables measurements of
low levels of BP. The device automatically inflates and deflates at a
rate that is preset from 1 to 6 mm Hg per heartbeat per second
and indicates invalid readings due to factors such as movement
artifacts and noise. Pediatric, adult, and obese cuffs were used
according to the arm size of the participant. The device is connected
with a Baumanometer mercury column to permit simultaneous
BP readings. High correlations (0.99 and 0.93 for SBPs and DBPs,
respectively; P<0.001) were obtained between BP measured
manually and by the automated BP monitor for a single reading before
the rest period at the beginning of the mental stress protocol. 50 mm Hg above the baseline SBP. The mirror image tracing task
was then administered. During this task, subjects traced the outline of
a star via a mirror image (direct vision of the star was blocked by a
screen) as many times as possible in 3 minutes, and BP was measured at
30 and 120 seconds. The mirror image tracing task was chosen because it
tends to elicit an increase in peripheral
resistance19 and was used successfully in our
previous studies of middle-aged women.20
A Toshiba SSA-270A scanner equipped with a 5-MHz linear array
imaging probe was used. Sonographers, who were blind to the mental
stress testing, scanned the right and left common carotid artery,
carotid bulb, and the first 1.5 cm of the internal and external carotid
arteries. For each location, the sonographer imaged the vessel in
multiple planes and then focused on the interfaces required to measure
IMT and also on any areas of focal plaque. The best images were taped
and later digitized for scoring.
The last two measures of SBP, DBP, HR, and pulse pressure during
the initial resting period, the two measures during the mirror image
tracing task, and the two measures during the public speaking task were
averaged within period or task. Baseline values were subtracted from
task levels to yield individual task scores for illustrative purposes.
To have a baseline-free measure of stress responses, baseline values
were regressed onto each task level and standardized. Because mental
stress measures are more reproducible when responses to individual
tasks are summed, these standardized individual task residualized
scores were summed. 2. Then association of the plaque index and the
residualized stress scores was evaluated by one-way ANOVA with tests
for linear trend. With the use of logistic regression analyses,
we then examined those variables that were significant in the ANOVA
analyses independent of age, use of HRT, baseline BP or
HR at stress testing, ever-smoking status, and
triglyceride levels.
Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Characteristics of Sample
The women in the analysis were almost all white,
and a majority were currently married (Table 1
). The women were relatively well
educated, with approximately three fourths having at least some
college. At the time of the mental stress testing, the mean age of the
women was 55.7 years, with a range of 50 to 60 years; at the time of
the ultrasound scan, the mean age of the women was 57.6 years, with a
range of 52 to 62 years. A mean of 2.3 years separated the mental
stress and ultrasound assessments, (median, 2.9 years; range, 0 to 5.3
years). Approximately 40% of the women were on HRT at the time of the
mental stress protocol.
View this table:
[in a new window]
Table 1. Sample Characteristics
(n=254) 2. The Spearman correlation
between mean IMT and the plaque index was r=0.49,
P<0.001. ). The magnitude of the changes
in BP and HR is comparable to that obtained in our laboratory among
middle-aged women, although the increase in SBP during mirror image
tracing is somewhat greater than previously observed. As in other
studies,20 the increase in SBP and HR was greater
during the public speaking task than during the mirror image tracing
task. This pattern is thought to reflect a greater myocardial response
during public speaking and a greater resistance response during mirror
image tracing. The Pearson correlations between the two task levels,
adjusted for the common baseline level, were 0.55, 0.24, 0.39, and 0.38
(P<0.01) for SBP, DBP, pulse pressure, and HR,
respectively.
View this table:
[in a new window]
Table 2. BP and HR During Mental Stress
Testing
Greater IMT was associated with higher resting SBP and pulse
pressure and lower resting HR (Table 3).
The magnitude of the increase in pulse pressure during both tasks
combined (and adjusted for baseline pulse pressure) was positively
related to IMT (Figures 1 and 2) both because of a nonsignificant
positive association of stress-induced SBP as well as nonsignificant
negative association of stress-induced DBP. An examination of the
associations separately by task showed that pulse pressure residualized
change was positively associated with IMT and DBP change was negatively
associated with IMT during the mirror image tracing task.
View this table:
[in a new window]
Table 3. Pearson Correlations Between IMT and Mental Stress
Measure
View larger version (12K):
[in a new window]
Figure 1. Mean pulse pressure change scores during mirror
image tracing task of women partitioned into four nearly equal groups
according to the distribution of IMT scores.
View larger version (13K):
[in a new window]
Figure 2. Mean pulse pressure change scores during speech
task of women partitioned into four nearly equal groups according to
the distribution of IMT scores. ). Logistic regression showed that after
adjustment for potential confounders, relative to women with a plaque
score of 1 or 0, women with a plaque score of 2 were at risk for a
lower DBP residual mirror image tracing score (B=0.32,
P<0.04; odds ratio=1.37; confidence interval, 1.02 to 1.84)
and for a higher pulse pressure residual mirror image tracing score
(B=0.38, P=0.01; odds ratio=1.47; confidence
interval, 1.09 to 1.97).
View larger version (17K):
[in a new window]
Figure 3. Mean pulse pressure and DBP change scores during
mirror image tracing task of women according to their plaque
index.
Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
This study sought to evaluate the hypothesis that stress-induced
changes in cardiovascular responses were related to
early carotid atherosclerosis in middle-aged women. The
sample entered the study in 1983 to 1984 free of hypertension,
insulin-dependent diabetes, and other diseases requiring long-term
pharmacological treatment and, at the time of stress testing starting
in 1993, were free of medications known to influence the
cardiovascular system. The stress testing was
administered several years before the ultrasound testing and included
measures of BP and HR during the mirror image tracing task and public
speaking. Results showed that baseline measures of SBP and pulse
pressure were related to IMT, a finding previously reported in the
present group.12 21 More importantly for our
purposes, IMT was related to the magnitude of change in pulse pressure
summed across tasks, independent of age, use of HRT, baseline measures
of pulse pressure, smoking status, and triglyceride levels.
Independent of the same covariates, the plaque index was related to
pulse pressure change but only during the mirror image tracing task.
Taken together, these findings suggest that a large pulse pressure
response to mental stress is an important predictor of subsequent
IMT.
Selected Abbreviations and Acronyms
BP
=
blood pressure
CHD
=
coronary heart disease
DBP
=
diastolic blood pressure
HR
=
heart rate
HRT
=
hormone replacement therapy
IMT
=
intima-media thickness
SBP
=
systolic blood pressure
Acknowledgments
This study was supported by National Institutes of Health grants
HL-28266 and HL-40962.
Footnotes
Reprint requests to Karen A. Matthews, PhD, Department of Psychiatry, University of Pittsburgh, 3811 O'Hara St, Pittsburgh, PA 15213.
References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
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A. Steptoe, M. Cropley, J. Griffith, and C. Kirschbaum Job Strain and Anger Expression Predict Early Morning Elevations in Salivary Cortisol Psychosom Med, March 1, 2000; 62(2): 286 - 292. [Abstract] [Full Text] [PDF]
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M. J. Domanski, B. R. Davis, M. A. Pfeffer, M. Kastantin, and G. F. Mitchell Isolated Systolic Hypertension : Prognostic Information Provided by Pulse Pressure Hypertension, September 1, 1999; 34(3): 375 - 380. [Abstract] [Full Text] [PDF]
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A. Rozanski, J. A. Blumenthal, and J. Kaplan Impact of Psychological Factors on the Pathogenesis of Cardiovascular Disease and Implications for Therapy Circulation, April 27, 1999; 99(16): 2192 - 2217. [Abstract] [Full Text] [PDF]
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M. Zureik, P.-J. Touboul, C. Bonithon-Kopp, D. Courbon, C. Berr, C. Leroux, and P. Ducimetiere Cross-Sectional and 4-Year Longitudinal Associations Between Brachial Pulse Pressure and Common Carotid Intima-Media Thickness in a General Population : The EVA Study Stroke, March 1, 1999; 30(3): 550 - 555. [Abstract] [Full Text] [PDF]
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