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1 Institute of Neuroscience and 4 Department of Physiology, Tzu Chi College of Medicine and Humanities, Hualien 970; 2 Department of Neurology, Tzu Chi Buddhist General Hospital, Hualien 970; 3 Yu-Chi Health Station, Nan-Tou 555; 5 Community Medicine Research Center, National Yang-Ming University, Taipei 112; and 6 National Research Institute of Chinese Medicine, Taipei 112, Taiwan, Republic of China
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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To clarify the influence of gender on
sympathetic and parasympathetic control of heart rate in middle-aged
subjects and on the subsequent aging process, heart rate variability
(HRV) was studied in normal populations of women
(n = 598) and men
(n = 472) ranging in age from 40 to 79 yr. These groups were divided into eight age strata at 5-yr intervals
and were clinically diagnosed as having no hypertension, hypotension,
diabetic neuropathy, or cardiac arrhythmia. Frequency-domain analysis
of short-term, stationary R-R intervals was performed, which reveals
very-low-frequency power (VLF; 0.003-0.04 Hz), low-frequency power
(LF; 0.04-0.15 Hz), high-frequency power (HF; 0.15-0.40 Hz),
the ratio of LF to HF (LF/HF), and LF and HF power in normalized units
(LF% and HF%, respectively). The distribution of variance, VLF, LF,
HF, and LF/HF exhibited acute skewness, which was adjusted by natural logarithmic transformation. Women had higher HF in the age strata from
40 to 49 yr, whereas men had higher LF% and LF/HF between 40 and 59 yr. No disparity in HRV measurements was found between the sexes in age
strata 
60 yr. Although absolute measurements of HRV (variance, VLF,
LF, and HF) decreased linearly with age, no significant change in
relative measurements (LF/HF, LF%, and HF%), especially in men, was
detected until age 60 yr. We conclude that middle-aged women and men
have a more dominant parasympathetic and sympathetic regulation of
heart rate, respectively. The gender-related difference in
parasympathetic regulation diminishes after age 50 yr, whereas a
significant time delay for the disappearance of sympathetic dominance
occurs in men.
autonomic nervous system; gender difference; frequency domain analysis
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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HEART RATE VARIABILITY (HRV) has been categorized into high-frequency (HF), low-frequency (LF), and very-low frequency power (VLF) ranges according to its frequency (26). HF is equivalent to the well-known respiratory sinus arrhythmia and is considered to represent vagal control of heart rate (10). LF is jointly contributed by both vagal and sympathetic nerves (3). The ratio LF/HF is considered by some investigators to mirror sympathovagal balance (1, 20) or to reflect the sympathetic modulations (18, 20, 22, 26). Because it is accessible and noninvasive, frequency-domain analysis of HRV has gained its popularity with broad applications as a functional indicator of the autonomic nervous system (ANS). For example, HF has been shown to decrease in diabetic neuropathy (19, 26), whereas LF/HF is sensitive to postural change (20) and mental stress (23). Our laboratory has recently demonstrated that LF and HF are decreased by pentobarbital anesthesia in the rat (32). In a human study, we found that LF is eliminated in brain death (16) and can be used as a prognostic tool for the prediction of patient outcome in the intensive care unit (33). In contrast to the well-documented changes of HRV in response to many pathological states, however, we were surprised to find that the effect of gender on HRV is still unclear. For example, women have been reported to have a lower (30), similar (6), and higher (13) HF than men. Even the effect of the aging process on the gender-related difference is uncertain.
Analyses of HRV have been recommended for both long-term (24 h) and short-term (5 min) studies (26). Although 24-h analysis of HRV (6, 30) is helpful in increasing the frequency resolution, especially for the lower frequency power, its application in a normal volunteer is difficult to accomplish. For example, changes in the physical or mental states of the study subjects (20, 23), changes in environments (23), and even noises in the ambulatory recordings (17) may severely influence the results of HRV analysis. Because the ANS, which regulates HRV, is very sensitive to changes in the internal or external environments of the body, a strict experimental control must be done to study HRV. For this purpose, 5-min recording is more practical than 24-h recording. Besides, HRV has been known to change along with aging (21, 24, 34), and the effects of aging on gender differences should also be considered. In this study, we proposed to systemically evaluate the effect of gender on resting HRV in eight age strata covering 40-79 yr on the basis of short-term (5-min) recording of an electrocardiogram (ECG) acquired in a well-controlled environment. From this study, we hoped to clarify the effect of the two basic physiological parameters, namely, sex and age, on the resting state of HRV, which is related to tonic ANS regulation of heart rate.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Study sample and experimental setup.
The procedures used in this study were approved by the Human Research
Committee of the National Yang-Ming University, Taipei, Taiwan. A total
of 1,070 normal volunteers (598 women and 472 men), ages 40-79 yr,
were randomly enrolled for this study. The population was distributed
into eight strata based on 5-yr age intervals (Table
1). We excluded subjects with the following conditions, which affect cardiovascular fluctuations (18, 26): hypotension (systolic pressure <110 mmHg or diastolic pressure <60
mmHg), hypertension (systolic pressure >140 mmHg or diastolic pressure >90 mmHg) (11a), diabetic neuropathy, an implanted cardiac pacemaker, frequent occurrence of atrial fibrillation, premature atrial
or ventricular contractions, or other forms of arrhythmia. Furthermore,
no patients were receiving medication or using drugs reported to
influence cardiovascular fluctuations, such as hypnotics or autonomic
blockers. Informed consent was obtained from each participant.
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Processing of ECG signals. The computer program for HRV analysis was modified from our previous method (16, 33) according to the recommended procedures (26). In the QRS identification procedure, the computer first detected all peaks of the digitized ECG signals using a spike detection algorithm (14) similar to general QRS detection algorithms. Parameters such as amplitude and duration of all spikes were measured so that their means and standard deviations (SD) could be calculated as standard QRS templates. Each QRS complex was then identified, and each ventricular premature complex or noise was rejected according to its likelihood in standard QRS templates. The R point of each valid QRS complex was defined as the time point of each heart beat, and the interval between two R points (R-R interval) was estimated as the interval between current and latter R points. In the R-R interval rejection procedure, a temporary mean and SD of all R-R intervals were first calculated for standard reference. Each R-R interval was then validated: if the standard score of an R-R value exceeded 3, it was considered erroneous or nonstationary and was rejected. The average percentile of R-R rejection according to this procedure was 1.2%. The validated R-R values were subsequently resampled and interpolated at the rate of 7.11 Hz to accomplish the continuity in time domain.
Frequency-domain analysis.
Frequency-domain analysis was performed using the nonparametric method
of fast Fourier transform (FFT). The direct current component was
deleted, and a Hamming window was used to attenuate the leakage effect
(15). For each time segment (288 s, 2,048 data points) our
algorithm estimated the power spectral density on the basis of FFT. The
resulting power spectrum was corrected for attenuation resulting from
the sampling and the Hamming window (25, 29). The power spectrum was
subsequently quantified into various frequency-domain measurements as
defined previously (Table 2) (26). In
particular, LF was normalized by the percentage of total power except
for VLF (total power 
VLF) to detect sympathetic influence on
HRV (LF%) (26). A similar procedure was also applied to HF (HF%). All
HRV parameters were expressed in original, square root, and natural
logarithmic form to demonstrate and correct possible skewness.
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Statistical methods.
Variance, VLF, LF, HF, and LF/HF were logarithmically transformed to
correct the skewness of distribution. Correlations among all parameters
were assessed using Pearson's correlation coefficient. The coefficient
of determination
(r2) between
two variables can be obtained by the square of their correlation
coefficient (r). We consider a good
or strong correlation between two variables at
r2 0.5 because
>50% of the change in one variable can be explained by the change in
the other. Correlation between each parameter and age was also assessed
using linear regression analysis. Differential effects of the two
genders and the eight age strata on HRV parameters were compared using
two-way ANOVA. When indicated by a significant F statistic, regional differences were
isolated using post hoc comparisons with Fisher's least significant
difference test. Comparisons between two sets of data were performed
with the unpaired Student's t-test.
Statistical significance was assumed for
P < 0.05. Values are expressed as
means ± SE.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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R-R interval and HRV measurements.
Whereas the distribution of the original R-R interval, LF%, and HF%
exhibited no significant skewness, the histograms of variance, VLF, LF,
HF, and LF/HF, however, were skewed significantly to the right (Fig.
1A).
The skewness in distribution of variance, VLF, LF, HF, and LF/HF could
be partially corrected by square root transformation (Fig.
1B) and could be further eliminated by natural logarithmic transformation (Fig.
1C).
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0.05). In other words, LF, either absolute or relative, was the
most independent HRV measurement of the basal R-R interval. All
of the absolute measurements were well correlated with each
other (r2 0.5). VLF exhibited the best correlation with variance
(r = 0.89), compatible with the fact
that the short-term variance is mostly contributed by VLF. LF% and
HF% were well correlated with LF/HF
(r2 0.5).
However, the correlations between the absolute and relative measurements of HRV were weak
(r2 < 0.5).
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Differential effects of sex and aging.
The age distribution for all participants was 59.4 ± 0.3 yr, which
was similar to that for individual male and female populations (60.1 ± 0.5 vs. 58.8 ± 0.4 yr). The female population had higher HF
and HF%, whereas the male population exhibited larger LF/HF and LF%
(Table 4). It should be mentioned that
there was no significant difference in mean arterial pressure between
the male and female populations.
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0.42),
with a coefficient of determination of 0.176, which means that 17.6%
of ln(LF) may be explained by age. When ln(LF) of the male and the
female populations was analyzed separately, the
r2 of female
population (0.202) was larger than that of the male population (0.152).
Similar findings were noted in other absolute measurements of HRV
(Table 5).
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60 yr.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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This study determined the various parameters of HRV in a large
population of normal humans between 40 and 79 yr of age, from which the
effects of gender and aging on cardiac sympathetic and parasympathetic
controls were evaluated. The neural regulation of heart rate was
analyzed by frequency-domain analysis of short-term HRV from subjects
at supine rest in the daytime. Among all standard HRV measurements
recently defined (26), we found that log-transformed LF best correlates
with age. Women had a higher HF in the age strata of 40-49 yr,
whereas men had higher LF% and LF/HF between 40 and 59 yr. There was
no disparity in any HRV measurements between genders in subjects age
60 yr. Although absolute measurements of HRV (variance, VLF, LF, and
HF) decreased linearly with age, no significant change in relative
measurements (LF/HF, LF%, and HF%), especially in men, was detected
until age 60 yr. We concluded that middle-aged women and men have a
more dominant parasympathetic and sympathetic regulation of HR,
respectively. The gender-related difference in the parasympathetic
regulation diminishes after age 50 yr, whereas there is a significant
time delay for the disappearance of sympathetic dominance in men. In
terms of frequency-domain analysis, it is also worthwhile to note that
among all short-term HRV measurements, the absolute measurements,
especially LF, better reflected the aging process, whereas relative
powers were superior at detecting the effect of gender.
It has been reported that HRV measured in subjects at supine rest in a quiet and relaxed atmosphere can be used as an assessment of vagal control of heart rate (10). More recently, transfer function analysis has shown that vagal control of heart rate can extend to both LF and HF. The sympathetic control, however, was limited to LF because of its frequency response (3). Therefore, the absolute measurements of HF in this study are considered to represent vagal control of heart rate, and LF is jointly contributed by sympathetic and parasympathetic nerves. Relative measurements (LF/HF, LF%, and HF%) appear to have provided quantitative evaluations of graded changes in the state of sympathovagal balance (1, 20). LF% and LF/HF have also been considered by previous investigators to reflect sympathetic modulation (18, 20, 22, 26). The physiological explanation of the VLF is much less defined (26). A recent study revealed that although VLF is influenced by the renin-angiotensin-aldosterone system, it depends primarily on the presence of parasympathetic outflow (27).
This study was undertaken to delineate the differential effects of gender and aging on frequency-domain parameters of short-term HRV based on a large population of normal humans. It is a complete comparison for all the short-term parameters, especially the relative powers, defined by the Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (26). An intriguing and novel finding in the present study was that absolute measurements of HRV better reflected the aging process, whereas relative measurements were superior in detecting the effect of gender. It also is interesting to note the finding that middle-aged women and men have a more dominant parasympathetic and sympathetic regulation of heart rate, respectively, and that this gender-related difference eventually disappears in the advanced age groups.
The gender-related differences in the ANS have been noted previously. For the parasympathetic system, it has been reported that estrogen has a facilitating effect on cardiac vagal function (8). In this study, 424 (71%) women were postmenopausal; the mean age of menopause was 47.7 yr with an SD of 4.7 yr. Only 6% of the postmenopausal women received hormone replacement therapy. Thus the disappearance of vagal dominance in women older than 50 yr is compatible with the hypothesis of the facilitating effect of female sex hormones on vagal function. On the other hand, men have been reported to have higher indexes of sympathetic function, including muscular sympathetic nerve activity (9), neuron number in sympathetic ganglia (2), and LF/HF of HRV (13). The dominance in sympathovagal balance of men may also contribute to a higher cardiac mortality (31).
The opinions on gender-related difference in HRV are diverse in the literature. Bigger et al. (6) reported that men have larger LF and VLF than women, but they have similar HF. Huikuri et al. (13) reported that men have larger LF% and LF/HF but smaller HF. More recently, Umetani et al. (30) reported that HRV for all time-domain measurements is lower in women, especially below the age of 50 yr, and they believe the level of parasympathetic activity is lower in young women. Our result for middle-aged subjects is compatible with that of Huikuri et al. (13). We found that men exhibited larger LF/HF and LF% than women in the age strata of 40-59 yr, but women had higher HF in the age strata of 40-49 yr. The discrepancy between these studies may be partly due to the different experimental variables. Bigger et al. (6) and Umetani et al. (30) acquired ECG readings using a 24-h Holter monitor, whereas we and Huikuri et al. (13) collected ECG readings of subjects at supine rest in a quiet environment. Under the latter conditions, vagal activity becomes the major contributor to HRV (10), whereas sympathetic activity may contaminate LF of HRV, especially in an upright posture (20). Thus our results support the finding that the vagal modulation of HR is augmented in middle-aged women compared with men. In our study, the sympathetic dominance of men can be better demonstrated by LF/HF and LF% in the age strata >50 yr, when the vagal indexes (e.g., HF and variance) between both genders are similar.
Respiratory sinus arrhythmia was reported to decrease age dependently in time-domain analysis, and this was subsequently confirmed by frequency-domain analysis (24, 34). We found that all indexes of vagal modulation of HR decline continuously with age, especially in women. In the literature, the role of the aging process in sympathetic modulation is more controversial. The catecholamine concentration has been reported to increase with age, whereas the receptor activity is downregulated (21). The LF/HF of HRV has been found to remain unchanged with age (34). In this study, however, LF/HF and LF% were found to decline significantly after age 60 yr, especially in men. Thus it is notable that sympathetic and parasympathetic modulations of HR appear to have different patterns in response to aging.
Although generated by complex interaction of sympathetic and parasympathetic functions, LF (log transformed) has the best correlation with age, indicating the advantage of LF over other HRV measurements in predicting the aging process of the ANS. In previous studies, LF was also found to be superior as a predictor of mortality (4, 6, 29, 33) and in the diagnosis of brain death (11, 16). Thus the combined analysis of sympathetic and vagal functions by LF is revealed to be more accurate in the prediction of mortality and aging. Unlike respiratory sinus arrhythmia, LF is not directly influenced by respiration, but it has been proposed that LF is generated from a complex feedback mechanism in the baroreflex loop (7). The finding that LF has the least correlation with basal R-R among all absolute measurements of HRV (Table 3) further indicates that LF is an independent index to basal cardiac rhythm.
Most current applications analyze absolute measurements of HRV without any mathematical (log, square root) transform. However, it had long been noted that HRV measurements seem to distribute in a nonnormal pattern, most likely logarithmic normal (5). In some studies, the HRV measurements have been square root transformed (12). The application of mathematical transform should be determined by the distribution pattern of each parameter. We therefore made a complete comparison for all short-term measurements of HRV under a variety of mathematical transforms (Fig. 1). We found that the distributions of original variance, VLF, LF, HF, and LF/HF were severely skewed, which could best be corrected by logarithmic transform. We also found that all absolute measurements of HRV and LF/HF correlated more significantly with age in their logarithmic transforms. These findings support the theory that absolute measurements of HRV should be log transformed to achieve normal distribution. Although normalized powers (LF% and HF%) also yield significant physiological information, the shapes of their distributions are less often discussed. Our data indicate that distributions of LF% and HF% are more like normal distributions and that the use of mathematical transform is not necessarily applicable.
The observation of respective dominances of parasympathetic modulation in women and sympathetic modulation in men before old age is interesting. It is compatible with the lower prevalence of cardiovascular disease in women before menopause in comparison with men. The complex age-gender interaction in the autonomic control of the heart and its relationship to cardiovascular diseases warrant further exploration.
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ACKNOWLEDGEMENTS |
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We thank Dr. Cyprian V. Weaver for assistance in preparing the manuscript.
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FOOTNOTES |
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This study was supported by National Research Institute of Chinese Medicine Grant NRICM-86112 and National Science Council (Republic of China) Grant NSC-87-2314-B-320-006-M04.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: T. B. J. Kuo, Institute of Neuroscience, Tzu Chi College of Medicine and Humanities, Hualien 970, Taiwan, Republic of China (E-mail: tbjkuo{at}mail.tcu.edu.tw).
Received 9 February 1999; accepted in final form 23 July 1999.
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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, Male; 
, female. Values
are means ± SE; nu, no units (normalized).
* P < 0.05;
P < 0.01 between genders
by Student's t-test.