Journal of Gerontology: MEDICAL SCIENCES
2000, Vol. 55A, No. 6, M329–M335
Copyright 2000 by The Gerontological Society of America
Effects of Aging on Cardiovascular Responses to
Gravity-Related Fluid Shift in Humans
Chihiro Miwa,1 Yoshiki Sugiyama,2 Tadaaki Mano,1 Toshiyoshi Matsukawa,1
Satoshi Iwase,1 Takemasa Watanabe,3 and Fumio Kobayashi2
1Department
of Autonomic Neuroscience, Research Institute of Environmental Medicine, Nagoya University, Japan.
2Department of Health and Psychosocial Medicine, Aichi Medical University, Japan.
3Department of Hygiene and Public Health, Osaka Medical College, Takatsuki, Japan.
Background. Fluid shift induced by postural change causes autonomic neural responses of the cardiovascular system
that buffer blood pressure fluctuation. The aim of the study was to clarify the effects of aging on cardiovascular autonomic functions in response to gravity-related fluid shift that unloads or loads the baroreceptors in human subjects.
Methods. A chest electrocardiogram, blood pressure by Finapres, and stroke volume by impedance method were
measured in healthy young men (23–31 years old) and healthy elderly men (74–80 years old) during supine rest, at 90⬚
head-up tilt and thermoneutral head-out water immersion. Spectral analysis was applied to the time series data of the
R-R intervals (heart rate variability [HRV]) and systolic blood pressure (blood pressure variability [BPV]). The arterial
baroreflex gain for heart rate was estimated using frequency transfer function analysis.
Results. The young subjects had stable blood pressure, despite the larger amount of fluid shift induced by both tilt
and immersion, and had marked changes in HRV and BPV. The elderly subjects failed to maintain stable blood pressure
during these perturbations, despite less fluid shift and no significant changes in HRV and BPV. The arterial baroreflex
gain for heart rate was not changed in the elderly subjects, whereas the gain decreased with upright in the young subjects
and showed an increasing tendency during immersion compared with upright posture.
Conclusions. These findings suggest that the adaptivity of the autonomic nervous system to gravity-related fluid
shift is reduced in elderly people, and this may cause blood pressure instability.
G
RAVITY is a natural physical stimulus that humans
live with. It affects cardiovascular function because we
change posture in our active daily life (upright, sitting,
squatting, and lying), which influences hydrostatic pressure
gradient from the foot to the head. Changing one’s posture
resets the hydrostatic pressure gradient, and a gravity-related
fluid shift is produced along the Gz axis. This shift induces
neural responses of the autonomic nervous system that regulate cardiovascular functions to buffer blood pressure fluctuations induced by postural changes.
Head-up tilt induces a fluid shift from the upper to the
lower part of the body, resulting in a decrease in stroke volume. To compensate for the hypotensive effect of reduced
stroke volume, heart rate and vascular resistance are increased by enhancing both cardiac and vasomotor sympathetic nerve activities and suppressing cardiac vagal activity
through the unloading of arterial and cardiopulmonary
baroreceptors (1,2). In contrast, head-out water immersion
induces cephalad fluid shift, resulting in an increase in cardiac filling and loading mainly of the cardiopulmonary
baroreceptor. Slowing the heart rate and reducing vascular
resistance buffer the hypertensive effects of the increased
stroke volume by enhancing cardiac vagal activity and suppressing sympathetic nerve activity (3). These buffering effects of autonomic nerve activity contribute to maintaining
stable blood pressure.
Some investigators have tried to relate the autonomic nervous function with aging by using a spectral analysis
method. Advancing age results in diminished heart rate
variability (HRV), whereas the spectral powers for blood
pressure variability (BPV) are greater in elderly persons
than in those who are young and middle when supine or
standing (4–7). However, there is no report about the effects
of aging on responses in heart rate and blood pressure during both head-up tilt and head-out water immersion. It is important to determine how the age-related changes in the autonomic nervous system correlate with gravity-related fluid
shift in elderly persons.
To clarify the effects of aging on the autonomic responses to gravity-related fluid shift, the cardiac sympathovagal balance and vasomotor sympathetic nerve activity were estimated noninvasively by applying spectral
analysis to HRV and BPV during head-up tilt and head-out
water immersion. In addition, arterial baroreflex gain for
heart rate was also evaluated by applying frequency transfer
function analysis with coherence analysis (8).
METHODS
Subjects
Sixteen healthy men, aged 23 to 80 years, were divided
into two groups: the elderly group (8 men, aged 74 to 80
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MIWA ET AL.
years, 74.9 ⫾ 2.7 years, mean ⫾ SD) and the young group
(8 men, aged 23 to 31 years, 25.3 ⫾ 2.8 years). The mean
weight and height for the elderly group were 60.0 ⫾ 6.4 kg
and 160.3 ⫾ 4.4 cm, and for the young group 69.1 ⫾ 7.4 kg
( p ⬍ .05 vs elderly) and 170.2 ⫾ 3.7 cm ( p ⬍ .05 vs elderly). The mean body mass index for the elderly group was
23.4 ⫾ 3.0 kg/m2 and for the young group 23.8 ⫾ 1.6 kg/m2
(not significant vs elderly). All subjects were nonsmokers
and took neither cardiovascular nor noncardiovascular
drugs. The elderly subjects were sports circle members and
were engaged in active daily work. The young subjects were
students at Nagoya University. Although physical activity
and energy expenditure were not measured, their activities
of daily living were not impaired. None of the subjects had a
history of renal disease, diabetes mellitus, or other diseases
that could affect the autonomic nervous function. They ate a
light breakfast without caffeine 3 hours before the experiments and refrained from eating and drinking anything from
2 hours before the experiments. Written informed consent
for participation in the study was obtained from each subject. This study was approved by the Human Research
Committee of Research Institute of Environmental Medicine, Nagoya University.
Protocol
We used the water immersion facilities at the Space Medicine Research Center, affiliated with the Research Institute
of Environmental Medicine, Nagoya University. The ambient temperature of the experimental room was maintained at
27 ⫾ 1.0⬚C with an air conditioner. The subject lay on a tilt
table with the right arm stretched on the table. We recorded
a chest electrocardiogram (ECG, lead CM5), noninvasive
continuous finger arterial pressure by Finapres (model
2300, Ohmeda, Louisville, CO), and intermittent blood
pressure in the left upper arm with an automatic sphygmomanometer (model BP-203NP, Colin Electronics, Komaki,
Japan). The ECG and arterial pressure wave form were
stored in a multichannel frequency modulation magnetic
tape recorder (model KS-616U, Sony-Magnescale, Tokyo,
Japan). The stroke volume was estimated by an impedance
cardiograph (model NCCOM3R7, BoMed Co., Irvine, CA),
and the digitized data were transmitted to a personal computer (model PC9801NV, NEC, Tokyo, Japan) through a
serial port RS-232C. The ECG, blood pressure, and impedance cardiogram were recorded in the horizontal supine position (supine) for 15 minutes. The tilt table was then inclined to 90⬚ so that the subject stood in an upright position
Figure 1. Upper panel: Original traces of the R-R interval (RRI) for an elderly and a young subject during supine, upright, and head-out water immersion conditions. Middle and lower panels: spectral density curves for heart rate variability (HRV) of the elderly subject (middle) and
the young subject (lower). In the elderly subject, there was faster fluctuation with a periodic cycle of several seconds duration, whereas in the
young subject the fast fluctuation occurred during supine and immersion postures, relatively slower fluctuation when upright.
SYMPATHOVAGAL RESPONSES AND AGING
on the foot plate with his hip strapped by a wide belt (upright). His right shoulder was abducted at 100⬚ to not wet
the finger cuff and the sensor. The upright position was
maintained for 5 minutes to record the variables. Thermoneutral water (34.5⬚C) was then added up to the acromion of
the subject while in the upright position (immersion). It took
about 5 minutes to raise the water level from the foot to the
acromion. We began to record the variables immediately after the water level reached the acromion, and this condition
was maintained for 5 minutes.
Data Analysis
The ECG and blood pressure wave form were played
back from the frequency modulation tape and converted to
digital data at the sampling frequency of 1,000 Hz through
an analog-to-digital converter (model ADX-98E, Canopus,
Kobe, Japan). Data from the last 2 minutes of the supine
rest, head-up tilt, and water immersion were used for frequency domain analysis. Temporal positions of the R-wave
peaks were detected on a personal computer (model PC9801DA, NEC, Tokyo, Japan). The original ECG, with
markers indicating the positions of all the detected R waves,
was scanned to eliminate falsely detected error peaks. After
confirmation of the positions of all the R-wave peaks, the
consecutive R-R intervals (RRI) were calculated from the
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temporal positions of the waves. Beat-to-beat systolic blood
pressure was obtained by detecting each systolic peak on
the digitized blood pressure wave form.
Spectral decomposition of HRV and BPV was performed by
the Maximum entropy method (MemCalc 1000, Suwa Trust,
Sapporo, Japan) on the respective time series data for the beatto-beat RRI and systolic blood pressure (9). This method is
superior to the fast Fourier transform in that it has higher spectral resolution and shorter time series data with no window
function. The optimum lag of the prediction-filter order for 2
minutes of data was determined as 35, on the basis of information criteria such as Akaike’s information theoretical criterion
and the characteristic correlation time. After calculating the
power spectral density, the magnitude of the power for HRV
and BPV was calculated by measuring the area under the
spectral density curve with the trapezoidal formula (10). The
values were divided into three major bands: very low frequency (VLF ⫺0.04 Hz), low frequency (LF 0.04–0.15 Hz),
and high frequency (HF 0.15–0.40 Hz) domains (11,12).
Frequency transfer function analysis with coherence analysis was performed using signal processing software DADisp/
Pro-32 with advanced DSP module (Version 4.1, Astrodesign, Kawasaki, Japan). Equidistant time series data with a
sampling frequency of 2 Hz were made from the time series
data of the beat-to-beat RRI and systolic blood pressure by
Figure 2. Average changes in the spectral power of heart rate variability in the three frequency domains for supine, upright, and head-out water immersion conditions. VLF: very low frequency; LF: low frequency; HF: high frequency; LF/HF ratio: ratio of the LF to the HF power. Values are means ⫾ SE. †p ⬍ .05 vs supine, *p ⬍ .05 vs upright, #p ⬍ .05 vs young subjects.
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MIWA ET AL.
applying cubic spline interpolation. After the DC elimination, frequency transfer function and coherence were calculated by Welchian method with a real data number of 128,
an overlapped data number of 112, and a data number of
256 for spectral decomposition. Arterial baroreflex gain was
estimated by calculating the mean value of the amplitude for
the transfer function when the coherence value was higher
than 0.5 in the high frequency domain (0.15–0.40 Hz) (8).
Statistical Analysis
Values are expressed as mean ⫾ standard error (SE). Differences in both between conditions and aging were analyzed by two-way factorial analysis of variance. When the
independent variables produced significant effects in the dependent variable, Fisher’s protected least significant difference was calculated. Significance was set at p ⬍ .05.
RESULTS
Changes in Heart Rate Variability
Representative original traces of RRI in one subject from
each group under the three conditions are shown in Figure 1,
together with the spectral density curves. Figure 2 summarizes
the changes in HRV for both groups under the three conditions. When supine, the VLF, LF, and HF powers of HRV
were significantly lower in the elderly group than those in the
young groups (VLF, 1,492.6 ⫾ 419.8 vs 414.7 ⫾ 111.0
ms2; LF, 696.8 ⫾ 127.6 vs 271.6 ⫾ 127.3 ms2; HF, 554.0 ⫾
210.2 vs 133.7 ⫾ 35.5 ms2; young vs elderly, p ⬍ .05). The
young subjects had significant changes in HRV in response
to upright and water immersion. VLF and HF powers were
reduced by head-up tilt (VLF, 1,492.6 ⫾ 419.8 vs 288.0 ⫾
67.7 ms2; HF, 554.0 ⫾ 210.2 vs 36.2 ⫾ 11.1 ms2; supine vs
upright, p ⬍ .05), with no consistent changes in LF power;
then the LF/HF ratio increased (1.9 ⫾ 0.3 vs 16.4 ⫾ 4.2; supine vs upright, p ⬍ .05). Immersion increased HF power
(36.2 ⫾ 11.1 vs 258.3 ⫾ 85.0 ms2; upright vs immersion, p ⬍
.05), with no significant changes in VLF and LF power. The
LF/HF ratio decreased, compared with the value in the upright position (16.4 ⫾ 4.2 vs 1.7 ⫾ 0.3; upright vs immersion, p ⬍ .05). For the elderly group there were no significant changes in the HRV among the three conditions.
Changes in BPV
Representative original traces of systolic blood pressure
in a subject from each group under the three conditions are
Figure 3. Upper panel: Original traces of systolic blood pressure (SBP) from an elderly subject and a young subject during supine, upright,
and head-out water immersion conditions. Middle and lower panels: spectral density curves of blood pressure variability (BPV) for the elderly
and young subject under the three conditions.
SYMPATHOVAGAL RESPONSES AND AGING
shown in Figure 3 together with the spectral density curves.
Figure 4 summarizes the changes in BPV in both groups under the three conditions. When supine, the VLF and LF
powers of BPV did not differ between the two groups, but
HF power was significantly higher in the elderly subjects
(1.5 ⫾ 0.3 vs 6.7 ⫾ 1.5 mmHg2; young vs elderly, p ⬍ .05).
With head-up tilt, the HF power of BPV significantly increased in the young subjects (1.5 ⫾ 0.3 vs 6.9 ⫾ 2.6
mmHg2; supine vs upright, p ⬍ .05). The elderly subjects
had an inverse response; a decrease in the HF power of BPV
(6.7 ⫾ 1.5 vs 2.0 ⫾ 0.2 mmHg2; supine vs upright, p ⬍
.05). Water immersion reduced the LF power of BPV in the
young subjects (18.4 ⫾ 4.1 vs 10.7 ⫾ 2.8 mmHg2; upright
vs immersion, p ⬍ .05), whereas the elderly group showed
no significant changes in any of the frequency domains.
Changes in Heart Rate, Blood Pressure, Stroke Volume,
and Cardiac Output
Changes in these variables in response to the gravityrelated fluid shift are given in Table 1. The young subjects
had an average increase in heart rate of 24 beats/min by the
postural change from supine to upright and a decrease of 20
beats/min during water immersion compared with upright
posture. The elderly subjects had an average increase in
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heart rate of 4 beats/min in response to upright, whereas
there was no change in heart rate by water immersion.
Blood pressure in the young subjects showed little
change during both upright posture and water immersion.
The elderly subjects had a higher systolic blood pressure
during supine posture and water immersion than did the
young subjects. Diastolic blood pressure decreased during
upright posture, and both systolic and diastolic blood pressures increased during water immersion in the elderly subjects. The young subjects showed a significant reduction in
stroke volume during upright posture and a significant increase during water immersion. There were no significant
changes in stroke volume in the elderly subjects during upright posture and water immersion, but stroke volumes
when supine and water immersion were lower in the elderly
than in the young subjects. Cardiac output was not significantly changed among the three conditions in both the
young and the elderly groups. The elderly subjects had consistently lower cardiac output under the three conditions
than the young subjects.
Changes in Arterial Baroreflex Gain for Heart Rate
Arterial baroreflex gains for heart rate in both groups under the three conditions are summarized in Figure 5. When
supine, the arterial baroreflex gain for heart rate was signifi-
Figure 4. Average changes in the spectral power of blood pressure variability in the three frequency domains for supine, upright, and headout water immersion conditions. VLF: very low frequency; LF: low frequency; HF: high frequency, LF/HF ratio: ratio of the LF to the HF power.
Values are means ⫾ SE. †p ⬍ .05 vs supine, *p ⬍ .05 vs upright, #p ⬍ .05 vs young subjects.
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MIWA ET AL.
Table 1.
Group
Young
Supine
Upright
Immersion
Elderly
Supine
Upright
Immersion
Changes in Heart Rate, Systolic and Diastolic Blood Pressure, Stroke Volume, and Cardiac Output
HR (beats/min)
SBP (mmHg)
DBP (mmHg)
SV (mL/beat)
CO (L/min)
64.5 ⫾ 2.0
88.2 ⫾ 3.9*
69.2 ⫾ 2.7†
118.0 ⫾ 2.8
122.0 ⫾ 3.0
122.3 ⫾ 1.0
64.0 ⫾ 2.8
67.0 ⫾ 2.0
67.3 ⫾ 2.0
121.7 ⫾ 9.2
77.5 ⫾ 5.5*
107.7 ⫾ 8.9†
7.8 ⫾ 0.6
6.8 ⫾ 0.5
7.4 ⫾ 0.6
65.2 ⫾ 3.6
69.3 ⫾ 4.8
67.7 ⫾ 3.8
134.6 ⫾ 5.5‡
131.7 ⫾ 6.8
138.5 ⫾ 5.5†‡
76.3 ⫾ 2.7‡
72.5 ⫾ 4.2*
76.4 ⫾ 5.5†
71.4 ⫾ 7.5‡
62.0 ⫾ 6.5
70.5 ⫾ 7.7‡
4.6 ⫾ 0.4‡
4.1 ⫾ 0.3‡
4.6 ⫾ 0.5‡
Notes: Values are means ⫾ SE (n ⫽ 8, young group; n ⫽ 8, elderly group). HR ⫽ heart rate; SBP ⫽ systolic blood pressure; DBP ⫽ diastolic blood pressure; SV ⫽
stroke volume; CO ⫽ cardiac output.
*p ⬍ .05 vs supine; †p ⬍ .05 vs upright; ‡ p ⬍ .05 vs young group.
cantly higher in the young subjects than in the elderly subjects (17.6 ⫾ 3.7 vs 6.1 ⫾ 2.6 ms/mmHg; young vs elderly,
p ⬍ .05). The arterial baroreflex gain for heart rate was decreased by the postural change from supine to upright in the
young subjects and showed a significant increase during
water immersion compared with head-up tilt (17.6 ⫾ 3.7 vs
2.6 ⫾ 0.4 ms/mmHg; supine vs upright, p ⬍ .05). On the
other hand, the elderly subjects showed no significant
changes in the gain among these three conditions.
DISCUSSION
Our study examines the effect of the aging process in humans on cardiovascular autonomic functions. We induced
two kinds of gravity-related fluid shifts in human subjects,
head-up tilt and head-out water immersion, which respectively unload and load the baroreceptors. The elderly subjects failed to maintain stable blood pressure during these
perturbations, despite less fluid shift and no significant
changes in HRV, BPV, and the arterial baroreflex gain for
heart rate, which were estimated by frequency domain anal-
Figure 5. Average changes in the arterial baroreflex gain for heart
rate in the high frequency domain for supine, upright, and head-out
water immersion conditions. Values are means ⫾ SE. †p ⬍ .05 vs supine, #p ⬍ .05 vs young subjects.
ysis. Thus, our study suggests that the adaptivity of the autonomic nervous system in response to gravity-related fluid
shift is reduced in elderly people and that this poor autonomic response may be in part related with the impaired
baroreflex function.
Effects of Aging on Autonomic Responses to
Gravity-Related Fluid Shift
The gravity-related fluid shift caused by head-up tilt produces a decrease in central blood volume and unloads the
baroreceptors. In the young subjects, unloading of the
baroreceptors caused the cardiac sympathovagal balance to
become sympathetic predominant and vasomotor sympathetic nerve activity to increase, resulting in stable blood
pressure in the face of a large fluid shift. On the other hand,
elderly people have been described to have consistently
lower spectral powers for HRV during supine rest and headup tilt (6,7). In this study, the elderly subjects had lower
power for HRV throughout the frequency range considered
in this study. However, the changes in LH/HF ratio were not
altered by the postural change from supine to upright. Moreover, the VLF power for BPV in the elderly subjects
showed no difference from that in the young subjects. These
observations are at odds with previous studies, which reported that LH/HF ratio for HRV increased similarly in both
young and elderly people by head-up tilt and that the VLF
power for BPV is larger in elderly people (6,7,11). Data
length analyzed from the present study is shorter than theirs.
We applied head-up tilt using a tilt table with the help of a
belt, so this condition differed from active standing. In addition, the right shoulder was abducted at 100⬚ so as not to wet
the finger cuff and the sensor. These factors could have possibly affected the results.
Head-out water immersion induces a cephalad fluid shift
(13–15) that loads baroreceptors, eliciting activation of cardiac vagal activity and relative suppression of cardiac and
vasomotor sympathetic nerve activities to compensate an
increased cardiac filling (3,16). There is little in the literature that discusses the neural control of systemic circulation
during head-out water immersion, especially in elderly people. Elevation of blood pressure in elderly people during immersion, despite less fluid shift, was reported by Stachenfeld and coworkers (5) and by Tajima and coworkers (17).
In a previous study, we reported that vasomotor sympathetic
nerve activity, recorded as muscle sympathetic nerve activity,
SYMPATHOVAGAL RESPONSES AND AGING
was suppressed by head-out water immersion in the young
subjects and that the suppression of muscle sympathetic
nerve activity by immersion is reduced with advancing age
(3). In the present study, blood pressure was significantly
elevated in the elderly subjects with a lack of buffering autonomic responses, in spite of less fluid shift. Our present
findings confirm the previous findings, that elderly subjects
show a lesser buffering effect of the autonomic functions.
Arterial Baroreflex Function in the Elderly Subjects
We assessed the arterial baroreflex gain for heart rate by
applying frequency transfer function analysis with coherence
analysis to clarify whether the arterial baroreflex function is
involved in the blood pressure instability and less autonomic
response to gravity-related fluid shift. As reported previously,
the sensibility of arterial baroreflex for heart rate decreased
by postural change from supine to upright (8,18). Moreover,
the sensitivity was increased significantly during immersion
compared with the upright position in the young subjects.
Thus, the young subjects showed an adaptive response of
baroreflex function to the evoked gravity-related fluid shift.
The decreased sensitivity may maintain higher heart rate,
compensating for the hypotensive effect of a reduced stroke
volume during head-up tilt. Unlike the young subjects, the
elderly subjects showed no changes in the arterial baroreflex gain for heart rate among the three conditions. Thus, in
elderly subjects the impaired adaptive response of arterial
baroreflex function for heart rate to the evoked gravity-related
fluid shift may cause inappropriate autonomic responses, resulting in an instability of systemic blood pressure.
Limitations
We applied frequency domain analysis to BPV and impedance cardiography. These methods are indirect estimates
of vasomotor sympathetic nerve activity and stroke volume
respectively. Vasomotor sympathetic nerve activity can be
directly recorded using a microneurographic technique as
muscle sympathetic nerve activity. In a previous study, we
recorded muscle sympathetic nerve activity during head-out
water immersion from subjects aged 19 to 67 years (3).
Stroke volume or central venous pressure can be also measured by echocardiography or intravenous catheterization
into the thorax. It may be hard for elderly people to undergo
these operations during head-up tilt and water immersion.
We therefore calculated only the arterial baroreflex gain for
heart rate. Another arterial baroreflex function to control vasomotor sympathetic nerve activity and the cardiopulmonary baroreflex functions were not analyzed.
Although physical activity is known to affect the cardiovascular function, physical activity and energy expenditure
were not measured in this study. Taylor and coworkers reported that there was little difference in blood pressure and
cardiovascular regulation
. between younger and older people who had the same VO2max (19). Thus, physical activity
should be taken into consideration for future studies.
Acknowledgments
We thank Hatsue Suzuki for her technical assistance.
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Address correspondence to Dr. Tadaaki Mano, Professor and Director,
Research Institute of Environmental Medicine, Nagoya University Furo-cho,
Chikusa-ku, Nagoya 461-8601, Japan. E-mail: [email protected]
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Received August 31, 1998
Accepted September 12, 1999
Decision Editor: William B. Ershler, MD