From the Departments of Psychiatry and Biobehavioral Sciences (I.B.G.,
G.B., D.S.) and Radiology (D.B.H.), University of California, Los Angeles, and
the Research Service, West Los Angeles VA Medical Center (G.B.), Los Angeles,
Calif.
Correspondence to Iris B. Goldstein, PhD, UCLA Department of Psychiatry, 760 Westwood Plaza, Los Angeles, CA 90024-1759. E-mail irisg{at}ucla.edu.
Methods—Casual and 24-hour ambulatory BPs and HR measurements
were taken of 144 elderly individuals, aged 55 to 79 years. Subjects
had no evidence of previous health disorders. MRI scans of white
matter, subcortical gray matter, and insular subcortex were coded for
severity of hyperintensities.
Results—Mean casual BP for the group was 120/72 mm Hg. With
age and sex accounted for, individuals with the highest severity rating
of white matter hyperintensities had higher casual, awake, and sleep
systolic BPs; higher awake diastolic BPs; greater
awake systolic BP variability; and a smaller nocturnal fall in
systolic and diastolic BPs than individuals with
less severe ratings. Higher severity ratings for subcortical gray
matter hyperintensities were associated with elevations in casual,
awake, and asleep systolic BPs and a smaller HR drop during
sleep. Subjects with higher ratings for the insular subcortex had
higher systolic and diastolic BPs (casual, awake,
and asleep), greater HR variability during sleep, and a smaller
nocturnal fall in HR.
Conclusions—Casual and 24-hour ambulatory BPs and some ambulatory
HR measures are associated with subcortical lesions of the brain.
Longitudinal studies are needed to further explore the relationship
between white matter lesions and cardiovascular
measures, as well as the significance of these lesions for
cerebrovascular disease in healthy elderly subjects.
Most BP information on the elderly has been obtained by means of
standard clinic BP assessment. However, with the aid of 24-hour
ambulatory monitoring one can track BP during both awake and sleep
periods and obtain information on BP variability and falls in nocturnal
BP. For example, in a study of elderly subjects who had either never
been on antihypertensive medication or had not been taking it for 4
weeks, MRI abnormalities were associated with elevated ambulatory BP, a
small nocturnal fall in BP, and a lower HR.8
Using both casual and ambulatory assessments in the present study,
we evaluated the relationship between BP and HR and T2 HI in 144
healthy, active, unmedicated elderly men and women with no evidence of
previous BP, cardiovascular, psychological, or
neurological disorders.
Initial Screening
Medical Evaluation and Final Screening
The Mini Mental State Examination9 screened out
cognitive disorders (scores of <23), and the Brief Symptom
Inventory10 screened out individuals with
possible psychiatric symptoms. Subjects scoring >5 on the short form
of the Geriatric Depression Scale11 were also
excluded. The Spielberger Trait Anxiety Scale12
was administered for use as a covariate in later analyses.
Ambulatory Monitoring
Ambulatory data were first edited for artifact based on Accutracker
reading codes (insufficient ECG or Korotkoff sounds) and extreme values
(>200/120 or <70/40 mm Hg). Editing was done entirely by set
rules.15 Far outside values were excluded by the
box plot program of Systat. For each subject ambulatory measures for
SBP and DBP included mean values of awake and sleep periods.
Classification of each reading as awake or asleep was based on diary
entries and post-session reports. Only nighttime sleep values were
included in the sleep category.
In addition to averaging casual BP and HR for 2 days, mean values for
the following ambulatory measures were averaged over two 24-hour time
periods: awake level, asleep level, awake variability, asleep
variability, and percent drop during sleep. Change in BP or HR from
awake to sleep divided by the awake value [(awake-asleep)/awake]
represented percent drop. For a given subject, variability
was based on the standard deviation of the awake and of the asleep
periods for a given day. All data were based on a single day and
averaged over 2 days.
Activity Monitor
MRI Evaluation
MRI Ratings
Interobserver reliability was tested by rerating a subset of 27 scans
and comparing the results of two independent raters. Intraclass
correlation coefficients were computed by estimating variance
components associated with between-subject and within-subject
variabilities. The coefficients reflect the proportion of total
variance accounted for by differences among subjects. Significance of
the intraclass correlations was determined by the general linear model,
with subjects forming the grouping factor. Reliability coefficients
(intraclass r) were highly significant (P<.0001)
for HI severity ratings for the three regions: white matter
(r=.90, F=18.6); insula (r=.85, F=12.3); and
subcortical gray matter (r=.88, F=16.3).
Subjects' scans of HI of white matter, subcortical gray matter (basal
ganglia and thalamus), and insular subcortex were all rated on the
basis of intensity, size, and confluence of lesions. The absence of HI
in a particular brain region was rated as zero.
Representative examples of the lesions for the three
nonzero ratings are shown in the Figure
Data Analysis
White Matter HI
Subcortical Gray Matter HI
Insular Subcortex HI
Influence of Other Variables
DeCarli et al7 looked at white matter
lesions in 51 nonhypertensive subjects with low casual BPs (124/78
mm Hg), but this sample consisted of young and elderly subjects with a
much greater age range (19 to 91 years) than our sample. Their results
indicated that both age and SBP were predictive of white matter HI
volume. Other than being associated with age and hypertension, the
significance of white matter changes in individuals without
neurological problems is not completely
understood.4 19 Since white matter changes are
frequently detected in individuals over 60 years of age and are
considered part of the aging process, their significance has been
questioned. However, in a recent review Pantoni and
Garcia20 concluded that subjects with HI were at
increased risk of cerebrovascular events and deficits in some cognitive
functions. Longitudinal studies of healthy populations would contribute
to an understanding of the significance of HI. Also, the association
between BP and white matter lesions is more likely to be found for SBP
than for DBP.4 5 The Copenhagen City Heart
Study21 indicated that casual SBP was a stronger
predictor of stroke than DBP. Our results confirm the relationship
between casual SBP and white matter HI (Table 2
In addition to showing casual BP differences, our analyses of
T2 HI indicated that subjects with varying severity ratings exhibited
differences in ambulatory BPs. In general, the higher the severity
rating for white matter HI the higher the awake and asleep SBP and DBP
(Table 2
As SBP increased, ratings for subcortical gray matter HI indicated
greater severity, although only the two extreme ratings (mild/moderate
versus none) were significantly different from each other (Table 3
In their relationship to the insular subcortex,
cardiovascular factors displayed a somewhat different
pattern. Here both SBP and DBP (casual, awake, and asleep) showed
fairly large and highly significant differences between subjects with
mild to moderate rating and those with ratings of none. Subjects with
higher ratings had greater HR variability during sleep and a smaller
nocturnal HR fall than those with no insular subcortex HI. These
results agree with findings that the insular cortex has numerous
interconnections with the limbic system, hypothalamus, and other areas
of autonomic control. Patients with infarction of the insular cortex
have been shown to have higher norepinephrine levels and a
decreased or abolished fall in nocturnal BPs.27
There is evidence that the insular cortex mediates
cardiovascular changes and that there may be a pathway
within the lateral hypothalamic area linking the insular cortex with
the heart.28
The interpretation of these findings should be made in the context of
the specific population sampled. This was a relatively
homogeneous group of healthy, highly educated people who
were primarily nonsmokers and who exercised frequently.No major health
disorders had been diagnosed in the group nor had cases of hypertension
been previously diagnosed. All medical test results were within the
normal range. Even in these subjects, however, elevations in BP
(primarily within the normotensive range) were associated with
increased severity of T2 HI. In general, the higher the severity rating
the greater the casual BPs (particularly SBP). In addition, further
information was obtained by recording 24-hour ambulatory BP and
HR. BP during awake and asleep periods, BP and HR variability, and
nocturnal falls in BP and HR all showed relationships to T2 HI.
Of particular interest is the fact that BP and HR differences occurred
not only between subjects with extreme HI ratings but also between
those in the none and minimal categories. Although in only a few
instances were these cardiovascular differences
significant, there was a fairly consistent trend for BP to be
higher in subjects with minimal severity of lesions of the subcortical
gray matter and the insular subcortex when compared with subjects who
had no HI at all. Apparently, small BP elevations can be associated
with MRI changes in the elderly that are rarely of concern to
radiologists. Moreover, the fact that elderly individuals with BPs at
the upper normal ranges, and not just those with hypertension, may be
at risk of brain damage has implications for modifications in lifestyle
(ie, weight reduction, exercise, and dietary changes) in these men and
women.14 Effective and early control of BP may do
much to delay or even prevent onset of changes in the brain. It has
been predicted that decreasing DBP by 2 mm Hg would lead to a
17% decrease in hypertension and a 15% drop in the risk of stroke and
transient ischemic attacks.29 Moreover,
recent findings showed that three quarters of all strokes occurred in
subjects with SBPs of <144 mm Hg and DBPs of <95
mm Hg.30 More concern needs to be focused on
subjects within the upper normotensive ranges of BP.
Received September 19, 1997;
revision received January 30, 1998;
accepted January 30, 1998.
© 1998 American Heart Association, Inc.
Original Contributions
Relationship Between Blood Pressure and Subcortical Lesions in Healthy Elderly People
Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Background and Purpose—The
relationship between blood pressure (BP) and heart rate (HR) and MRI
assessments of subcortical T2 hyperintensities was evaluated in healthy
elderly men and women.
Key Words: blood pressure • elderly • heart rate • magnetic resonance imaging
Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
The single most
important risk factor for cardiovascular and
cerebrovascular disease for all age groups is
BP.1 2 Investigators have shown that particularly
among the elderly hypertensive patients have a relatively high
incidence of lacunar infarcts and white matter hyperintensities when
compared with normotensive subjects.3 4 5 However,
it may not be necessary for BP to be in the hypertensive range for it
to be considered a risk factor. Data from insurance studies indicate
that there is a gradient of ratios of actual to expected mortality that
increases with elevations in SBP.6 Even in
nonhypertensive individuals 19 to 91 years of age, higher casual SBP
was associated with a greater volume of white matter
HI.7
Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Subjects were recruited by media advertisements and from senior
centers in Los Angeles. Potential participants had to be healthy men
and women aged 55 to 80 years who were living in the community. From a
total of 1154 people inquiring about the study, 187 were not interested
and 758 did not meet the criteria. Fifty-nine subjects were dropped
after the medical examination, 3 were later dropped for noncompliance,
and MRIs could not be obtained for 3 subjects. The final sample
consisted of 144 subjects. All subjects gave informed consent, with
approval obtained from the Human Subjects Protection Committee of the
University of California, Los Angeles. Eligible subjects underwent
medical examinations and were scheduled to begin ambulatory BP
monitoring a few days later. They were studied during two 24-hour time
periods, on weekdays, about a week apart. At the end of the procedures
MRIs were recorded. Procedures are elaborated below.
All subjects went through extensive screening, beginning with
telephone contact. Initial exclusions involved subjects' reports of
any serious current or prior illness, history of hypertension, drug or
alcohol abuse, head injuries, obesity (body mass index>30
kg/m2), prior psychiatric illness, or any
medications influencing either the cardiovascular or
central nervous system. We also excluded anyone who had first-degree
relatives with Alzheimer's disease, schizophrenia, or
Huntington's chorea.
On their first visit, subjects were given a physical and mental
status examination by the project physician, including a complete
health history, 12-lead ECG, urinalysis, and chemical panel. Laboratory
tests were done by standard techniques (SmithKline Beecham Clinical
Laboratories). Exclusion criteria included neurological (eg, history of
cerebrovascular accident, Parkinson's disease, or any serious
involvement of the central nervous system),
cardiovascular (eg, congestive heart failure,
myocardial infarction, history of coronary disease, atrial
fibrillation, or symptomatic ventricular
arrhythmias), respiratory (eg, symptomatic
bronchospastic diseases), renal (eg, elevated creatinine;
proteinuria), endocrine, and major psychiatric or other disorders.
Those with possible diabetes (fasting glucose of >115 mg/dL or a
glucose >200 mg/dL after 1 hour or >114 mg/dL after 2 hours of a
glucose tolerance test with 75 g of glucose) were also excluded.
Exclusions were based on medical examination, laboratory findings, and
subject's medical history.
The Accutracker II (Suntech Medical Instruments) was used for
24-hour ambulatory BP monitoring. It has been used widely in clinical
and research studies and has established reliability and
validity.13 After the subject was seated for 5
minutes and just before the ambulatory monitor hookup, we assessed
casual BP and HR. Three successive readings of BP were taken according
to standard assessments.14 Three readings were
also taken of radial pulse rate. The laboratory assistant then applied
the ambulatory monitoring cuff to the nondominant arm. On each
measurement occasion, single readings of SBP and DBP were
obtained.15 The ambulatory recorder was
programmed to operate three times an hour on a random schedule during
waking hours and once an hour during sleep. Actual time of awake and
sleep periods was noted in subject's diary. On the basis of the
subject's information, we obtained indices of quality of sleep, number
of times awakened, and number of hours slept. The Epworth Sleepiness
Scale was administered to assess the presence of daytime sleepiness.
This scale has also been found to significantly distinguish normal
subjects from patients with sleep disorders (ie, sleep apnea syndrome)
identified by polysomnography.16
An actigraph (Mini-Motionlogger, Ambulatory Monitoring Inc) was
used to record frequency of movements in 1-minute intervals during
each 24-hour period of ambulatory monitoring. Using a custom computer
program (prepared by Timothy Elsmore, PhD), we obtained measures of the
average activity level for sleep and for awake periods and for the
10-minute period preceding each BP reading. The activity monitor was
used to confirm the differentiation of asleep from awake readings and
to account for the effects of activity on BP and HR.
Imaging Protocol
MRI was performed using a Picker 1.5T instrument with an imaging
protocol consisting of four sequences. The initial spin-echo sequence
(TR, 100 msec; TE, 30 msec; 10 mm thickness) of a coronal pilot
image with one signal averaged was used to evaluate symmetrical
positioning of the head. If a subject's head was tilted noticeably
laterally, the subject was repositioned and a new coronal pilot image
was acquired. The image was then used to align the acquisition grid of
the subsequent sagittal images. Pilot sagittal images were obtained
from a second spin-echo sequence (TR, 550 msec; TE, 26 msec; 5 mm
thickness) with two signals averaged. To obtain a true midsagittal
image, the middle slice of this series of 28 images was aligned on the
coronal pilot.17 The remaining sagittal images
visualized the entire brain, and were used to determine the position of
the two subsequent axial sequences in order to image the entire brain
in the axial plane from the apex to the inferior ends of
the temporal lobes. A transverse dual spin-echo sequence (TR, 2500
msec; TE, 20 and 90 msec) with 256x192 view matrix, 25-cm field of
view, and two signals averaged was used to acquire the 3-mm thick
contiguous axial images used in the ratings of HI. This sequence was
performed twice to visualize the entire brain.
The images were rated visually for areas of HI by two of us
(D.H. and G.B.), both blinded to other research data on the subjects.
Ratings of T2 HI were made without regard to clinical significance, and
only HI identified on both early and late echo images were rated. In
the evaluation of focal HI the raters selected abnormal foci and
avoided including expected HI, such as those produced by partial
voluming of sulcal cerebrospinal fluid or uniform round cortical
vessels appearing in typically anticipated positions within sulci. 
. A rating of 1
involved minimal changes rarely mentioned in radiology reports because
they are generally deemed to be of no significance for patients over 55
years of age. A rating of 2 was defined as definite brain tissue
changes of mild severity and of questionable significance. Moderate
changes that were felt to be significant indicators of a possible
disease process received a rating of 3. In this population there were
no very severe HI. In some instances there were fewer than 10% of
subjects in the grade 3 category (13 subjects had a 3 rating for
subcortical gray matter HI; 4 subjects had a 3 rating for insular
subcortex HI). These subjects were combined with those who had a rating
of 2 into a mild/moderate category (Tables 3 and 4).
View larger version (162K):
[in a new window]
Figure 1. Representative slices exemplifying how HI
were rated. Grade 0 is not included and contains no HI. A rating of 1
has minimal changes, rating 2 involves mild changes, and rating 3
indicates moderate changes. Arrowheads point to rated T2 HI. The
following areas were rated: top panel, white matter HI (image 3 has
many large HI); middle panel, subcortical gray matter HI; and lower
panel, insular subcortex HI (arrows define region that extends medially
to lateral border of the putamen).
View this table:
[in a new window]
Table 3. Casual and Ambulatory BP and HR Differences for
Ratings of Subcortical Gray Matter HI
View this table:
[in a new window]
Table 4. Casual and Ambulatory BP and HR Differences for
Ratings of Insular Subcortex HI
We performed a series of ANOVAs of casual and ambulatory BPs and
HR in a one-way group design (group=severity of lesion). Since both
dependent and independent measures were influenced by age and sex, they
were included as covariates in the analysis. Bartlett's test
showed that all of the variances in all analyses were
homogeneous. When the overall F was significant
(P<.05), Tukey tests were used to determine between-group
differences.
Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Subject Characteristics
The sample consisted of 82 women and 62 men, aged 55 to 79 years,
living in the community (Table 1). Racial
composition was 112 Caucasians, 20 Asian Americans, 11 African
Americans, and 2 Latinos. Only 5 subjects were current smokers. While
the majority was retired, 36% were still employed. Subjects exercised
about 10 hours per week and were highly educated, and almost half
earned over $50 000 per year. Elevations in casual BP were restricted
to 10% of the sample: 1 subject had stage 1 (mild) hypertension
(154/94 mm Hg); 1 had stage 2 (moderate) hypertension
(165/103 mm Hg); and 13 had isolated systolic
hypertension (SBP 140 to 152 mm Hg, DBP 69 to 88 mm Hg).
Among those with systolic hypertension, 7 subjects had SBP
between 140 and 143 mm Hg. The remainder of the subjects were
within the normotensive range. (For definitions of hypertension see
Reference 1414 .)
View this table:
[in a new window]
Table 1. Characteristics of Sample
In general, the higher the severity rating of white matter HI the
higher the level of BP during casual measurements as well as during
awake and sleep periods (Table 2). This
was particularly true for SBP, in which significant differences between
moderate and either none or minimal ratings ranged from 7 to 14
mm Hg. Although DBPs tended to show similar differences, only the
ambulatory DBP difference during awake periods was significant. Also,
subjects with the highest ratings had consistently higher BP
variability during awake and asleep periods than subjects in the other
rating categories, but significance was found only for SBP variability
during awake periods. Greater severity was also associated with a
smaller percentage drop in SBP and DBP from awake to asleep. HR was not
significant.
View this table:
[in a new window]
Table 2. Casual and Ambulatory BP and HR Differences for
Ratings of White Matter HI
Although all BP levels went up with increasingly higher ratings,
only SBP was significant (casual measurements and ambulatory
recordings while awake and asleep; Table 3
). Differences between the two extreme
groups (none and mild/moderate) varied between 6 and 10 mm Hg.
DBP effects were not significant. In addition, the nocturnal HR
decrease was less in the group with the greatest severity. None of the
variability measures were significant.
Both SBP and DBP (casual, awake, and asleep) had highly
significant findings with regard to HI of the insular subcortex (the
greater the rating the higher the BP) (Table 4). In comparisons of the extreme ratings
(none versus mild/moderate), SBP differences ranged from 8 to 13
mm Hg and DBP differences from 5 to 7 mm Hg. While BP
variability tended to increase with greater lesion severity, only HR
variability during sleep was significant. The fall in HR from being
awake to asleep was less in those subjects with the highest
severity.
Subsequent models were developed in which we considered the impact
of body mass index, anxiety, depression, and education on the
analyses, but they did not affect any of the findings.
Analyses of activity data during awake and asleep periods
indicated that awakening and rising during the night had no appreciable
effect on any of the ambulatory BP values. Using the actigraph method
of ruling out sleep readings classified as "awake" reduced the
number of readings used in calculations of BP and HR by 10% but had
very little effect on the mean values. Use of information on subjective
ratings of quality of sleep, number of hours slept, and number of
awakenings as covariates in analyses did not affect any of the
analyses. Also, no subjects scored within the range of
sleepiness encountered in patients with moderate or severe sleep apnea,
nor were BP variables related to performance on the Epworth
Scale.
Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Despite the large numbers of statistical tests, most tests showed
a consistent relationship between BP level and clinical ratings
of severity of MRI T2 HI. In general, the more severe the rating the
higher the BP (see Tables 2 through 4). Although other investigators
have found similar results with white matter lesions in hypertensive
patients, this is the first time that such a relationship has been
reported in a large sample of elderly people with such low BPs. The
casual mean BP for the group (120/72 mm Hg) contrasts sharply
with that of the general population mean of individuals between the
ages of 55 and 74 years (140/83 mm Hg).18
Although a diagnosis of hypertension had never been made in any of the
subjects, their current pressures would lead to a diagnosis of stage 2
hypertension in 1, stage 1 hypertension in 1, and isolated
systolic hypertension in the remaining
13.14 In the subjects with systolic
hypertension, SBP was relatively low for this age group (140 to
152 mm Hg). It is interesting to note that the 1 subject with
stage 2 hypertension had ratings of mild for subcortical gray matter
and insular subcortex HI but had no white matter HI. Although we did
not initially select individuals with such low BP, the sample resulted
from the stringent exclusion criteria used in obtaining this group of
healthy elderly men and women. Apparently a primary component of good
health as one ages is the maintenance of a low BP. ). However, casual DBP
followed a similar (although nonsignificant) trend in that subjects
with greater lesion severity had higher BPs. ). As with the casual BP, the greatest and most highly
significant differences for ambulatory measures were found for SBP. The
fact that BP remained relatively high during sleep indicates that BP
elevations were fairly consistent throughout the day. Moreover,
subjects with highest lesion severity were more likely than the other
subjects to exhibit smaller decreases in nocturnal SBP and DBP and to
have the greatest SBP variability while they were awake. Investigators
found that elderly subjects with multilacunar lesions and higher grades
of cerebrovascular damage (many with hypertension) had higher office
and ambulatory BPs, particularly during sleep, and a smaller fall in BP
during sleep than those with fewer cerebrovascular
symptoms.8 Particularly among hypertensive
patients, there was a higher prevalence of
cardiovascular complications in individuals whose BPs
failed to fall at night compared with those who showed decreased
nocturnal BPs. The maintenance of a "continuous pressure
overload" may contribute to the progression of left
ventricular
hypertrophy.22 Our results on
variability are somewhat unique, because Shimada et
al23 found no relationship between ambulatory
24-hour variability and white matter lesions. However, the importance
of variability is implied by the association in a number of studies
between increased BP variability and high prevalence of
cardiovascular target organ
damage.24 ).
Not only did subjects with HI have higher casual SBPs than those with
ratings of none but SBP was higher during both awake and sleeping
hours. The only other significant variable was percent fall in HR,
indicating that the mild/moderate group had a smaller nocturnal HR
fall. Howard et al25 found that in a group of 35
community-dwelling elderly subjects, subcortical gray matter HI were
associated with increases in SBP and DBP. Furthermore, hypertension has
been found to be a risk factor for lobar and basal ganglia primary
cerebral hemorrhage.26
Selected Abbreviations and Acronyms
BP
=
blood pressure
DBP
=
diastolic BP
HI
=
hyperintensities
SBP
=
systolic BP
TE
=
echo time
TR
=
repetition time
Acknowledgments
Support for this study was provided by Research Grant AG-11595
from the National Institute of Aging.
References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
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 G. Bartzokis, I. B. Goldstein, D. B. Hance, M. Beckson, D. Shapiro, P. H. Lu, N. Edwards, J. Mintz, and P. Bridge The Incidence of T2-Weighted MR Imaging Signal Abnormalities in the Brain of Cocaine-Dependent Patients Is Age-Related and Region-Specific AJNR Am. J. Neuroradiol., October 1, 1999; 20(9): 1628 - 1635. [Abstract] [Full Text]
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