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1 Division of Higher Nervous
Control, Muscle sympathetic nerve activity (MSNA)
was measured directly along with blood pressure at rest in 69 healthy
women (20-79 yr old) and 76 age-matched healthy men (16-80 yr
old). All were nonobese and normotensive. In the women and men the MSNA
was positively correlated with age (women:
y = 0.788x
aging; men; menopause; women
AN AGE-RELATED INCREASE in sympathetic nerve activity
has been established on the basis of earlier observations of
age-related increases in plasma norepinephrine concentration as well as
increases in directly recorded muscle sympathetic nerve activity (MSNA) using a microneurographic method (4-6, 14-16, 20). However, it is not known how gender influences the age-related increase in
sympathetic nerve activity. The available information on this issue is
based mainly on plasma norepinephrine concentrations (2, 5, 6, 21).
These data have been in part inconsistent and, thus, have failed to
provide a clear explanation of the influence of gender on sympathetic
activity. Although direct recordings of MSNA would provide a more
definitive approach to this issue, few such data are available. Ng et
al. (14) measured MSNA in 17 younger subjects (aged 19-30 yr) and
15 older subjects (aged 60-74 yr) and reported an age-related
increase in MSNA in resting subjects; they found that the gender
difference was an important determinant of MSNA at rest in the younger
and older subjects. There have been no studies evaluating the resting
MSNA in younger, middle-aged, older, and aged men and in women before,
during, and after menopause.
In this study, to clarify how gender influences the age-related
increase in sympathetic nerve activity in humans, we determined the
MSNA at rest in groups of healthy, normotensive, nonobese men and women
of different ages.
Selection of subjects.
The subjects were 69 healthy women (20-79 yr old) and 76 healthy
age-matched men (16-80 yr old). We divided the women and men into
five groups by age: 16 women and 19 men <30 yr old, 11 women and 13 men 30-39 yr old, 14 women and 10 men 40-49 yr old, 13 women
and 12 men 50-59 yr old, and 15 women and 22 men General procedures.
Subjects were examined in the supine position throughout the study
session. Systolic, diastolic, and mean blood pressures were determined
intermittently every minute using an automatic sphygmomanometer (model
BP-203NP, Nihon Colin, Komaki, Japan). The heart rate was monitored by
electrocardiogram. MSNA was continuously recorded using the
microneurographic method (4, 10-14, 16, 18-20).
MSNA recording.
Multiunit recordings of MSNA were obtained from a muscle fascicle of
the tibial nerve at the popliteal fossa. To record MSNA, a tungsten
microelectrode, 100 µm in shaft diameter, with an uninsulated tapered
tip of 1-5 µm and impedance of ~3-5 M
ABSTRACT
Top
Abstract
Introduction
Methods
Results
Discussion
References
5.418, r = 0.846, P < 0.0001; men:
y = 0.452x + 12.565, r = 0.751, P < 0.0001). The regression
intercept of y was significantly lower
(P < 0.0001) in the women than in
the men, and the regression slope was significantly steeper
(P < 0.0001) in the women. The MSNA
was lower in women than in men among those <30
(P = 0.0012), 30-39
(P = 0.0126), and 40-49 yr old
(P = 0.0462) but was similar in women
and men among those 50-59 (P = 0.1911, NS) and 
60 yr old (P = 0.1739, NS). The results suggest that MSNA increases with age in women and men and that the activity is markedly lower in young women than in
men but is markedly accelerated with age.
INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References
METHODS
Top
Abstract
Introduction
Methods
Results
Discussion
References
60 yr old, and
we defined 41- to 55-yr-old women as the middle-aged women during
menopause. Menopausal status was confirmed by menstrual history. Women
were considered premenopausal if they had regular menstrual cycle
lengths and had not taken hormones orally in the past year. Women were
considered postmenopausal if they had not menstruated for 12 mo. All
were normotensive (blood pressure <140/90 mmHg) and otherwise healthy
on the basis of a detailed health questionnaire, physical examination,
and resting and maximal exercise electrocardiograms. Because the body
fat was demonstrated to affect MSNA in the women and men (8), we
selected nonobese subjects; their body weight ranged from 15 to
+15% of ideal body weight assessed by body mass index (BMI). They took
no medication for 2 wk before the study. The study protocols were
approved by the Human Research Committee of Research Institute of
Environmental Medicine, Nagoya University. Written informed consent was
obtained from each subject after a detailed explanation of the purpose of the study, the procedures, and the possible risks.
(no. 26-05-1, Frederick Haer, Brunswick, ME) was inserted manually through the skin.
The spike potentials were amplified (model DAM-6A, World Precision Instruments, New Haven, CT), monitored on an oscilloscope (model 5113, Tektronix, Beaverton, OR) and a loudspeaker, and recorded continuously
on magnetic tapes, which were later played back to analyze the MSNA.
The recorded activity was fed through a band-pass filter (model E3201A,
NF, Yokohama, Japan) with a bandwidth of 400-3,000 Hz. The
filtered neurogram was passed through an integrator with a time
constant of 0.1 s to obtain the mean voltage neurogram of MSNA (4,
10-14, 16, 18-20).
Experimental protocol.
Subjects did not eat for 3 h before the experiment. All experiments
were performed with the subjects in the recumbent position in a quiet
room. After a successful nerve recording had been obtained, MSNA, heart
rate, and systolic, diastolic, and mean blood pressures were monitored
while the subjects rested quietly for 30 min. When all variables were
stable, a 10- to 15-min nerve recording was obtained.
Analysis. For the quantitative analysis of MSNA, the mean voltage neurogram of MSNA was displayed together with the electrocardiogram on a multidot thermal recorder (model 8M14, San-ei, Tokyo, Japan). Records were divided into periods of 1-min each, and for each period the amount of nerve activity was determined from the tracing. Sympathetic bursts were identified by inspecting the mean voltage neurogram and are expressed as bursts per minute, according to previous studies (10-13). The values for MSNA, heart rate, and blood pressure obtained over the 10- to 15-min measurement period were averaged. Statistical analysis was performed by ANOVA with the unpaired Student's t-test (see Tables 1 and 4, Figs. 2 and 3). The relationship between age and MSNA in women and men was calculated by linear regression using the least-squares method and by comparisons of the two regression intercepts and two regression slopes (Fig. 1). Recently, body fat (7, 8) and blood pressure (10, 12, 20) were demonstrated to be closely related to MSNA in humans. Thus a matrix of correlation coefficients between BMI, mean blood pressure, and MSNA was obtained in the women and men (see Table 2). With a partial correlation analysis, the relationships between age and MSNA were examined while adjusting for the BMI or mean blood pressure (see Table 3). Moreover, for comparisons between women and men in MSNA adjusted for BMI or mean blood pressure (see Fig. 3) and for comparisons between premenopausal and postmenopausal women in MSNA adjusted for age, BMI, or mean blood pressure, an analysis of covariance (ANCOVA) was performed. Statistical significance was defined as P < 0.05. Values are means ± SE, correlation coefficient, or P value (except for n and ranges of ages).
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RESULTS |
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Abstract
Introduction
Methods
Results
Discussion
References
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Subject characteristics and levels of cardiovascular variables at rest
are presented in Table 1. The heights of
the women were significantly less than those of the men, and the body
weights were significantly lower in the women (except for 60 yr).
There was no significant difference in BMI between the women and the men. There were no significant differences in systolic, diastolic, and
mean blood pressures or the heart rate between men and women, except
among those 30-39 yr old. Among those 30-39 yr old, the systolic (P = 0.0378), diastolic
(P = 0.0493), and mean blood pressures
(P = 0.0145) were higher in the men
than in the women, but the heart rate was similar in the two groups.
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There were positive relationships between age and MSNA in the women and men (Fig. 1). The MSNA at rest became progressively higher with advancing age in the women (P < 0.0001) and men (P < 0.0001). The regression intercept of y was significantly lower (P < 0.0001) in the women than in the men, and the regression slope was significantly steeper (P < 0.0001) in the women (Fig. 1). There were significant positive correlations between age, BMI, or mean blood pressure and MSNA in the women and men (except between BMI and MSNA in men; Table 2). In addition, there were significant positive correlations between age and MSNA adjusted for BMI (P < 0.0001) and for mean blood pressure (P < 0.0001) with partial correlation analysis (Table 3).
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There was a significant gender difference in MSNA; that is, the MSNA
was lower in the women than in the men among the subjects <30
(P = 0.0012), 30-39
(P = 0.0126), and 40-49 yr old
(P = 0.0462), but it was similar in
the women and the men among those 50-59 (P = 0.1911, NS) and 60 yr old
(P = 0.1739, NS; Fig.
2). For the comparisons between women
and men in MSNA adjusted for BMI or mean blood pressure, an ANCOVA was
performed (Fig. 3). In MSNA adjusted for
BMI and for mean blood pressure, there was also a significant gender
difference (Fig. 3). That is, the younger women had lower MSNA values
but the older women had MSNA values similar to those of the age-matched
men.
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In the middle-aged women (41-55 yr) we compared the levels of cardiovascular variables and MSNA at rest before and after menopause (Table 4). There were no significant differences in age, height, weight, BMI, or heart rate between premenopausal and postmenopausal women, but systolic (P = 0.0105), diastolic (P = 0.0256), and mean blood pressures (P = 0.0298) and MSNA (P = 0.0009) were significantly higher in the postmenopausal than in the premenopausal women (Table 4). For the comparisons between women and men in MSNA adjusted for age, BMI, or mean blood pressure, an ANCOVA was performed. The MSNA was significantly higher in the postmenopausal than in the premenopausal women for the MSNA adjusted for age (41.3 ± 3.1 vs. 27.9 ± 2.5, P = 0.0040), for BMI (42.9 ± 3.0 vs. 26.8 ± 2.5, P = 0.0005), and for mean blood pressure (43.2 ± 3.5 vs. 26.5 ± 2.8, P = 0.0022).
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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In this study we determined the MSNA at rest in groups of healthy,
normotensive, nonobese men and women of different ages. There were some
key observations. First, the MSNA was significantly increased with age
in the women and the men. The regression intercept was significantly
lower in the women than in the men, and the regression slope was
significantly steeper in the women. Second, the MSNA was lower in the
women than in the men among the subjects <30, 30-39, and
40-49 yr old but was similar in the women and the men among those
50-59 and 60 yr old. Third, in the middle-aged women the MSNA
was significantly higher in the postmenopausal than in the
premenopausal women of the same age.
The finding of increases in MSNA with advancing age in humans agrees with previous reports (4, 14, 16, 20). In the present study we also confirmed that MSNA is increased with age in women as well as in men. The mechanisms responsible for this increase, however, are not yet clear. Regarding the mechanism involved, the results of a recent investigation by Ebert et al. (4) fail to support the hypothesis that a reduced arterial baroreceptor reflex buffering of sympathetic outflow is responsible for the age-related rise in MSNA. Other hypotheses that remain to be directly tested in humans include decreased cardiopulmonary baroreceptor reflex inhibition of sympathetic outflow (1) and a non-baroreceptor reflex-related elevation in central sympathetic discharge rate (14).
Previous reports on the age-associated increase in MSNA have been based
on data obtained only from men (4, 16) or in groups comprised primarily
of men (16, 20). Moreover, studies using plasma norepinephrine
concentrations as an estimate of the absolute level of sympathetic
nervous system activity at rest also failed to provide definitive
insight into the potential influence of gender (5, 6, 21). These plasma
norepinephrine studies have suggested that sympathetic nerve activity
is not different (5, 21), higher (6), or lower (2) in women than in men
of similar age. The results of the present study demonstrate that for
younger, middle-aged, and older adult humans at rest, the MSNA is
significantly lower in younger women (<50 yr) than in men of the same
age but is similar in older women and older men (>50 yr). Recently,
Ng et al. (14) measured MSNA in 17 younger subjects (aged 19-30
yr) and 15 older subjects (aged 60-74 yr) and reported
progressively higher MSNA values in the young women, young men, older
women, and older men, i.e., an age-related increase in MSNA in resting
subjects, and that the gender difference was an important determinant
of MSNA at rest in the younger and the older subjects. For younger
subjects, our results agree with those Ng et al., but there is a
difference in results regarding older subjects between our study and
theirs. Our present study found that the MSNA was similar between women
and men not only at 60 but also 50-59 yr old. The reason for the
difference in results is not clear but could depend on sociocultural
differences between Japanese and American populations (e.g., life
history, diet), which could influence MSNA. We consider that MSNA is
lower in younger women (<50 yr) than in men but is similar in older
women and older men (>50 yr). In the present study, however, the MSNA values tended to be higher in older women rather than similar to those
of the age-matched men (Fig. 2). There is a possibility that a larger
group of older men and women may reveal a true gender difference; i.e.,
older women may have a higher MSNA than older men.
In our present study we also found lowered sympathetic nerve activity in younger women and premenopausal middle-aged women and markedly increased activity in postmenopausal middle-aged women and older women. Other investigators demonstrated that the resting levels of plasma norepinephrine were significantly higher in postmenopausal than in premenopausal women (9). However, they did not examine age-matched subjects; i.e., they compared the resting levels of plasma norepinephrine between premenopausal and postmenopausal women (36.7 ± 0.9 vs. 55.7 ± 1.1 yr, P < 0.01). Until now there had been no studies evaluating resting MSNA in younger, middle, older, and aged men and women, including before, during, and after menopause. The mechanisms of lowered sympathetic nerve activity in younger women and premenopausal middle-aged women and markedly increased activity in middle-aged postmenopausal women and older women are not clear, but the following possible mechanism can be offered. Recently, it was suggested that in postmenopausal women (9) and men (3) the sympathetic responses to psychological stress were reduced during the replacement of estrogen. They measured plasma norepinephrine levels before and during psychological stress tasks in postmenopausal women and observed that the increases in plasma norepinephrine levels induced by the stress tasks were reduced after the administration of estrogen compared with after treatment with placebo (3, 9). Moreover, Tollan et al. (17) suggested that progesterone reduced sympathetic tone in men. They measured the plasma norepinephrine concentrations in men before and during the administration of progesterone and showed that plasma norepinephrine levels were reduced during the administration (17). Therefore, in younger and premenopausal women, the existence of two sex hormones, i.e., estrogen and progesterone, may be related to the lowered sympathetic nerve activity in these women. Conversely, in postmenopausal and older women the levels of estrogen and progesterone in blood were significantly reduced, and the reduced levels of the two hormones may be related to the elevation of sympathetic nerve activity in these women.
In summary, we found that 1) in women and men, the sympathetic nerve activity increased with advancing age, and especially in women this activity may be markedly accelerated with age, 2) younger women had lower sympathetic nerve activity than did the younger men, but sympathetic nerve activity was similar in older women and older men, and 3) the sympathetic nerve activity was significantly higher in the postmenopausal than in the premenopausal middle-aged women.
Perspectives
In the present study, to determine how gender influences the age-related increase in sympathetic nerve activity in humans, we observed MSNA at rest in 69 healthy women (20-79 yr) and 76 age-matched healthy men (16-80 yr). The results suggest that MSNA increases with age in women and men and that among women the MSNA is markedly lower in young women than in men but markedly increases with age, implying that MSNA is accelerated during or after menopause. However, we cannot conclude the effects of age, gender, and menopause on sympathetic nerve activity from only the present and previous studies. In the future, larger studies and longitudinal studies, e.g., 10- or 20-yr follow-up studies, are necessary to establish the effects of age, gender, and menopause on sympathetic nerve activity in humans.| |
FOOTNOTES |
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Address for reprint requests: T. Matsukawa, Dept. of Autonomic Neuroscience, Div. of Higher Nervous Control, Research Institute of Environmental Medicine, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan.
Received 24 November 1997; accepted in final form 4 June 1998.
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Methods
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Discussion
References
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; n = 69) and
men (
; n = 76) studied. Resting
MSNA was significantly correlated with age (women:
y = 0.788x 
