International Journal of Obesity (2004) 28, 27–33
& 2004 Nature Publishing Group All rights reserved 0307-0565/04 $25.00
www.nature.com/ijo
PEDIATRIC FOCUS
Effect of physical activity on autonomic nervous
system function in lean and obese children
N Nagai1 and T Moritani1*
1
Laboratory of Applied Physiology, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan
OBJECTIVE: The autonomic nervous system (ANS) is a key factor in the regulation of energy balance and body fat storage;
however, to what extent the physical activity during the childhood years contributes to variations in ANS function is still unclear.
The present study was designed to investigate the ANS activity in lean and obese children, focusing on the differences in physical
activity levels.
SUBJECTS: This study was performed on 1080 school children initially recruited to the present study. In all, 24 physically active
and 24 inactive obese children (Z120% of the standard body weight) were chosen as samples. Then, 24 lean-active and 24
lean-inactive children, who were matched individually in age, gender, height, and the amount of sports activity, were carefully
selected from the remaining children.
MEASUREMENTS: Physical activity was classified as the frequency of participation in after-school sports activities (active; Z3
times per week, inactive; nothing). The ANS activities were measured during the resting condition by means of heart rate
(HR) variability power spectral analysis, which enables us to identify separate frequency components, that is, low frequency
(LF; 0.03–0.15 Hz), reflecting mixed sympathetic (SNS) and parasympathetic nervous system (PNS) activity, high frequency
(HF; 0.15–0.5 Hz), mainly associated with PNS activity, and total power (TP; 0.03–0.5 Hz), evaluating the overall ANS activity.
The spectral powers were log transformed for statistical testing.
RESULTS: The lean-active group demonstrated lower resting HR as well as significantly higher TP, LF, and HF powers compared
to the remaining groups. In contrast, the obese-inactive group showed significantly lower TP (Po0.05 vs the remaining groups),
LF (Po0.05 vs the lean groups), and HF power (Po0.05 vs the lean groups), respectively. The obese-active and lean-inactive
groups were nearly identical in all spectral parameters. The correlation analysis revealed that TP among 48 inactive children was
significantly and negatively associated with the percentage of body fat (r ¼ 0.53, Po0.001); however, such correlation among
48 active children was modest (r ¼ 0.33, P ¼ 0.02).
CONCLUSION: Our data suggest that obese children possess reduced sympathetic as well as parasympathetic nervous activities
as compared to lean children who have similar physical activity levels. Such autonomic reduction, associated with the amount of
body fat in inactive state, might be an etiological factor of onset or development of childhood obesity. On the other hand,
regular physical activities could contribute to enhance the overall ANS activity in both lean and obese children. These findings
further imply that regular physical activity might be effective in preventing and treating obesity beginning in the childhood.
International Journal of Obesity (2004) 28, 27–33. doi:10.1038/sj.ijo.0802470
Keywords: childhood obesity; regular physical activity; autonomic nervous system; power spectral analysis; heart rate variability
Introduction
A global epidemic of obesity in children has been recognized
internationally1 and the upward trend in childhood obesity
has also been observed in Japan. An epidemiological annual
survey revealed that prevalence of obesity in school children
aged 6–11 y is steadily increasing at a rate of 0.3% per year,
*Correspondence: Dr T Moritani, Laboratory of Applied Physiology,
Graduate School of Human and Environmental Studies, Kyoto University,
Sakyo-ku, Kyoto 606-8501, Japan.
E-mail [email protected]
and approximately doubled over the last two decades.2 Fastpaced Westernizing as well as rapid social changes force the
pediatric population to live a more comfortable and
sedentary environment. In a sample of 8000 children from
Student Health Survey in Japan,3 approximately half of the
children aged 10–14 y went to cram schools after school
hours until late at night; the children aged 8–17 y were
watching television on an average of 2.5 h per day, and,
moreover, playing video games on an average of 1.5 h as
well. These data as well as previous study4 provided evidence
that the tendency to increase childhood obesity might be a
result of environmental and cultural changes related to
physical inactivity in daily life.5
Preventive effect of physical activity on obesity
N Nagai and T Moritani
28
Many individuals maintain their body weight within small
limits during long periods, and such highly precise control of
energy balance is achieved by several regulatory loops.
Previous data6,7 and pharmacological blockade studies8,9
suggest that the sympathetic nervous system (SNS) is one of
the most regulatory systems of energy balance, and altered
SNS activity may affect the amount of fat mass in humans.
Moreover, a series of our recent studies have shown that obese
young women possess significantly lower SNS activity against
various thermogenic perturbations, such as cold exposure,10
capsaicin-contained diet,11 and mixed food intake.12
The above studies,6–12 as well as other reports,13,14
indicated that a reduced absolute sympathetic activity or a
blunted sympathetic reactivity in certain physiological
conditions was found in adult obese subjects. Additionally,
in the pediatric obesity research field, our current study15
demonstrated that the obese children possess reduced SNS
activity, as shown in adult obese subjects, and such
autonomic depression is associated with the duration of
obesity. These data strongly support the hypothesis that a
low level of SNS activity leads to the onset or the
development of obesity. However, it is still uncertain as to
whether the low SNS activity is influenced by the other
heterogeneous factors, such as physical activity level, which
might lead to a different profile of sympathovagal activity.
The findings of several cross-sectional16–18 and interventional research19 have shown that increased physical activity
is associated with higher levels of overall autonomic nervous
system (ANS) activity in adults16–19 and obese children.20 Nevertheless, the findings regarding the physiological effect of
physical activity on the SNS have been far inconclusive.16–20
The inconsistency is thought to arise largely from the
difficulty in controlling the arrangement of variables
(including genetic differences, physical activity levels, the
degree of obesity, dietary and behavioral habits, and
emotional stress) and in adequately assessing the SNS
activity in human subjects of all age groups. Although the
SNS plays an important role in human obesity, to the best of
our knowledge, no research regarding the physiological
effects of both obesity and physical activity on SNS
activity among healthy children has been published. Moreover, that the extent of body fat alone in the inactive state
can influence overall ANS (including SNS and parasympathetic nervous system (PNS)) activity in children remains
unclear.
Therefore, in the present study, we evaluated the resting
ANS activity by means of the heart rate variability (HRV)
power spectral analysis in healthy nonobese and obese
school children, who were carefully classified into physically
active and inactive subgroups, respectively, and investigated
whether the SNS and the PNS activities were altered in obese
and/or in physically inactive children. We also examined a
physiological association between the amount of body fat
and the sympathovagal activities, to examine the essence of
the ANS alteration as a potential etiological factor of
childhood obesity.
International Journal of Obesity
Methods
Subjects
This research was performed on 1080 healthy Japanese
children (576 boys and 504 girls) aged 6–12 years in two
public elementary schools. The study protocol was approved
by the Institutional Review Board of Kyoto University
Graduate School. All children and their parents were carefully instructed about the present study, and all gave their
written informed consent to participate in the study. Prior to
obtaining any data from the children, the parents completed
a standardized health questionnaire prepared for the children, regarding past medical history, current health condition, diet, physical activity, duration of TV watching, and
other current lifestyles. The food consumption data were
collected through a day dietary record method, and each
data on the individual level were converted into energy and
nutrients by means of the up-to-date version of the Japanese
food-composition table.21 After measuring the height, the
body mass and the percentage of body fat were determined
using a bioelectrical impedance analyzer (Model TBF-534,
Tanita Corp, Tokyo, Japan). The analyzer has been used in
pediatric investigations, since it is a simple and noninvasive
technique and it produces a reasonable estimate for body fat
content in children.22 However, the analyzer should be used
with careful attention because of the limitations.22 Therefore, we carefully followed the testing procedures for
optimized utilization of the analyzer as follows: (1) All
measurements were performed in the morning (from 0900 to
1100 h) for 4 consecutive days in the mild weather season.
(2) Avoiding drinks, at least 2 h, before the measurement. (3)
Changing the school timetable to avoid attending physical
education class before the measurement. Body mass index
(BMI) was also calculated as the body mass divided by height
squared.
To verify whether the state of obesity and physical activity
have an effect on ANS activities, all obese and active (obeseactive; 23 boys and one girl) and all obese and inactive
children (obese-inactive; 8 boys and 16 girls) were selected as
samples. Subsequently, the same numbers of age-, gender-,
and height-matched lean-active and lean-inactive children
were selected randomly from the remaining children.
‘Obesity’ was defined based on the criterion previously used
in pediatric research, greater than 120% of the standard body
mass for Japanese children.2,23 Physical activity was estimated as the frequency of participation in after-school sports
club activities, to adduce examples, softball, succor, volleyball, and basketball, which were performed in the school
gym or ground. Some children participated in the lesson of
valet, karate, or judo at the private schools after school
hours. All sports can be categorized into aerobic exercise.
‘Active’ was defined as the frequency of their sports activities
being more than three times a week, and more than 60 min
each time. Moreover, the intensive activity hours were
obtained from the time-budget questionnaires. ‘Intensive
activity’ was defined as ‘intensive practice or exercise with
heart thumping’. On the other hand, no children regularly
Preventive effect of physical activity on obesity
N Nagai and T Moritani
29
engaged in various sports activities or exercises in inactive
groups. All the selected children were in good health and
had no personal or family history of cardiovascular disease,
diabetes mellitus, or other endocrine diseases, and did not
take any medications. The descriptive characteristics of the
children are presented in Table 1.
Experimental procedure
The children came to the temporary laboratory we set up in
the school infirmary at 0830 h. All experiments were
performed in the morning and the entire research project
lasted for 6 days in June. The room was temperature
controlled (251C), quiet and comfortable, with minimization
of arousal stimuli. After accurate skin preparation, the
subjects were instrumented with electrocardiogram (ECG)
electrodes and then rested for at least 15 min before the start
of the experiment.
After the resting period, the CM5-led ECG signals were
continuously recorded for 5 min while each child remained
seated in a chair and was breathing normally.24 This position
is considered as a suitable posture to reflect both SNS and
PNS activities from our previous studies.10–12,15,19,25–27 Moreover, it should be noted that, according to our previous
experiment15 as well as pediatric physiology,28 children’s
breathing frequency is generally higher than 0.15 Hz (nine
times per min). Thus, we assumed that, without controlling
the respiration rates during the ECG measurements, respiratory-linked variations in heart rate (HR) did not overlap with
low-frequency (LF) HR fluctuations (o0.15 Hz) from other
sources.
R–R spectral analysis procedure
Our R-R interval power spectral analysis procedures have
been fully described elsewhere,25–27 and require only minimal cooperation from children being tested by the simple
and noninvasive method. Briefly, the analog output of the
Table 1
ECG monitor (MEG-6100, Nihon Kohden, Tokyo, Japan) was
digitized via a 13-bit analog-to-digital converter (HTB 410;
Trans Era, South Orem, UT, USA) at a sampling rate of
1024 Hz. The digitized ECG signals were differentiated, and
the resultant ECG QRS spikes and the intervals of the
impulses (R-R intervals) were stored sequentially on a hard
disk for later analyses.
Before R–R spectral analysis was performed, the stored R–R
interval data were displayed and aligned sequentially to
obtain equally spaced samples with an effective sampling
frequency of 2 Hz,29 and displayed on a computer screen for
visual inspection. Then, the direct current component and
linear trend were completely eliminated by digital filtering
for the band pass between 0.03 and 0.5 Hz. The root-meansquare value of the R–R interval was calculated as representing the average amplitude. After passing through the
Hamming-type data window, power spectral analysis by
means of a fast Fourier transform was performed on a
consecutive 256-s time series of R–R interval data obtained
during the test.
Based on our previous investigation,19,25–27 the spectral
powers in the frequency domain were quantified by
integrating the areas under the curves for the following
respective band width: LF (0.03 and 0.15 Hz), jointly
mediated by both SNS and PNS activity; high frequency
(HF: 0.15 and 0.5 Hz), mainly associated with PNS activity;
and the total power (TP: 0.03 and 0.5 Hz), could reflect the
overall ANS activity. The spectral powers were then logarithmically transformed for statistical testing.30–32
Statistical analyses
All data are expressed as mean7s.d. Differences in physical
characteristics and the parameters regarding the ANS activity
between groups were tested by ANOVA with least significance test as Tukey analysis. Pearson’s simple correlations
were used to examine the relationship between the TP and
the percentage of body fat in active and inactive children. A
Physical characteristics of childrena
Lean
Obese
Variables
Active (n ¼ 24)
Inactive (n ¼ 24)
Active (n ¼ 24)
Inactive (n ¼ 24)
Age (y)
Gender (boy/girl)
Height (cm)
Body mass (kg)
BMI (kg/m2)
Body fat (%)
Duration of obesity (y)
Sports (times/week)
Sports (h/week)
Resting HR (bpm)
Energy intake (kcal/day)
Fat intake (g/day)
9.671.3
23/1
137.2710.7
32.577.4
17.071.4
16.472.1
0
4.171.2
487.17232.7
73.576.7
2160.17442.2
69.2713.8
9.471.8
8/16
135.0712.1
31.577.9
17.071.5
17.573.0
0
0c
0c
83.777.0d
2085.57284.5
68.0713.5
9.571.4
23/1
139.5711.6
45.5711.3b
23.072.5b
28.675.1b
3.971.3b
3.971.2
420.07145.6
84.1711.2d
1962.27341.5
68.5719.2
9.371.7
8/16
138.1711.7
47.3713.3b
24.373.4b
30.974.2b
3.771.9b
0c
0c
89.076.2d
1920.37335.4
64.6713.9
a
Mean7s.d. bPo0.001 vs lean groups. cPo0.001 vs active groups. dPo0.001 vs lean-active group, respectively (by one-way ANOVA combined with post hoc Tukey
test).
International Journal of Obesity
Preventive effect of physical activity on obesity
N Nagai and T Moritani
30
P-value of o0.05 was chosen as the level of significance. All
statistical analyses were performed using a commercial
software package (SPSS version 10.0J for Windows; SPSS
Inc., Chicago, IL, USA).
Results
Physical data
The physical characteristics of lean and obese children
including active and inactive subgroups, respectively, are
reported in Table 1. The body mass, BMI, and body fat were
significantly higher in obese groups than in lean groups, as
expected. There were no differences in the body mass, BMI,
body fat, and duration of obesity between obese-active and
obese-inactive groups. The resting HR was significantly lower
in the lean-active group compared to the remaining groups,
while age, gender, height, sports time, and intensive activity
was not different between lean-active and obese-active
groups.
Nutritional data
Dietary energy and fat intake are described in Table 1. The
energy intake in obese groups appeared to be lower than lean
groups; however, there was no statistically significant
difference among groups.
Power spectral data
Figure 1 represents typical sets of raw R–R interval and the
power spectral data obtained from an obese-inactive, obeseactive, lean-inactive, and lean-active child, respectively,
during the resting condition. According to visual inspection,
the lean-active child showed remarkably greater R–R variability ranges as well as overall spectral powers than the
remaining children. In contrast, the obese-inactive child
possessed obviously reduced ranges in R–R variability as well
as in both LF and HF frequency components of the power
spectrum compared to the rest of the children.
The group data indicated that there were significant
differences in the R–R spectral parameters between the
groups (ANOVA, LF: F ¼ 10.54, Po0.001; HF: F ¼ 12.62,
Po0.001; TP: F ¼ 15.66, Po0.001). Following the post hoc
Tukey analysis, it was revealed that the state of obesity has a
strong influence on all the spectral parameters (LF, HF, and
TP) in both active and inactive children. As shown in
Figure 2, the obese-active group showed significantly lower
LF (6.570.7 vs 7.170.5 ln ms2, Po0.01), HF (6.471.2 vs
7.370.7 ln ms2, Po0.01), and TP (7.370.9 vs 7.970.5 ln ms2,
Po0.01) than the lean-active group, and the obese-inactive
group had significantly reduced LF (6.170.7 vs
6.670.4 ln ms2, Po0.05), HF (5.970.7 vs 6.570.4 ln ms2,
Po0.05), and TP (6.870.6 vs 7.370.2 ln ms2, Po0.05) than
the lean-inactive group.
On the other hand, physical activity independently has an
effect on the spectral parameters in both lean and obese
children. As compared to inactive groups, the lean-active
group manifested significantly higher LF (7.170.5 vs
6.670.4 ln ms2, Po0.05), HF (7.370.7 vs 6.570.4 ln ms2,
Po0.01), and TP (7.9v0.5 vs 7.370.2 ln ms2, Po0.01) than
the lean-inactive group. Obese children also showed similar
results, that is, the obese-active group had a significantly
higher TP (7.370.9 vs 6.870.6 ln ms2, Po0.05) compared to
the obese-inactive group.
Correlation among parameters of HRV and body fat
In order to further examine the relationship between the
total spectral powers and the percentage of body fat, all
children were divided into active (n ¼ 48) and inactive
(n ¼ 48) groups based on the frequency of participation in
after-school sports activities. As shown in Figure 3, the TP
among 48 inactive children was inversely correlated with the
percentage body fat (r ¼ 0.53, Po0.001); however, weaker
correlation was shown among 48 active children (r ¼ 0.33,
P ¼ 0.02), suggesting that such autonomic activities were
greatly influenced by the amount of body fat in the inactive
state.
Discussion
Figure 1 A typical set of our computed-aided ECG R–R interval power
spectral analysis results obtained from obese-inactive (left), obese-active and
lean-inactive (middle), and lean-active child (right), respectively: raw R–R
interval (top) and the corresponding spectrum (bottom) from which various
ANS activity components are derived.
International Journal of Obesity
The present study provides two primary findings. First, obese
children possess reduced overall ANS activity, especially the
LF power region reflecting sympathetic influences, and the
extent of such autonomic reductions among inactive
children have a significant relevance to body fatness.
Preventive effect of physical activity on obesity
N Nagai and T Moritani
31
Figure 3 Relationship between TP and percentage of body fat among 48
active (left) and 48 inactive children (right), respectively.
Figure 2 Comparison of LF (top), HF (middle), and TP (bottom) in leanactive, lean-inactive, obese-active, and obese-inactive groups, respectively.
Results are expressed as mean7s.d. for each group. **Po0.01, *Po0.05 (by
one-way ANOVA combined with a post hoc Tukey test).
Second, regular sports activities contribute to enhancement
of the overall ANS activity in both lean and obese children.
The activity of SNS is implicated in the regulation of
energy homeostasis6 and modulation of glucose and fat
metabolism through both direct neural and hormonal
effects.33 Low SNS activity, therefore, has been shown
to lead to lower levels of energy expenditure, and,
consequently, to a positive energy balance and weight
gain.13 A causal linkage between altered ANS activity and
obesity cannot be confirmed; however, our findings are
partly confirmatory of the above theory, as well as our
previous investigation15 which shows that reduced SNS and
PNS activities exist in sedentary obese children. Even during
childhood, lower levels of PNS activity are related to cardiac
autonomic neuropathy in diabetic patients with poor
glycemic control,34 duration of diabetes,35 and high blood
pressure.36 Therefore, reduced ANS activity appearing in our
healthy obese children might be a possible early sign which
might affect the future cardiovascular and metabolic related
disorders.
Other intriguing findings obtained from the present study
were that physically active children showed greater overall
ANS activity compared with inactive children in both obese
and lean children, demonstrating that regular vigorous
sports might contribute to the activation of ANS. Moreover,
in order to avoid negative effects on future health of
children, physical activity might be indispensable to children, in particular obese children. In the present study, the
ANS activity was related to the percentage of body fat in the
inactive state; however, the relationship between ANS
activity and percentage of body fat was less clear in the
active state (Figure 3). Some active children including obese
children showed remarkably higher values of the TP,
indicating a beneficial effect of physical activity on the
ANS activation. On the other hand, some obese-active
children still had a lower level of TP despite their regular
sports activity. The results imply that some obese-active
children, who possessed lower TP, might have a possible
problem, such as autonomic disturbance by long duration of
obesity.15 Conceivably, the period of sports participation as
well as the intensity of sports activity can influence the ANS
activity; however, the details of the issue yet remain unclear.
Therefore, further study will be needed to scrutinize whether
sports activities have a long-term effect on the ANS activity
in the obese children. In the previous intervention study,19
we found a possibility that exercise training for 12 weeks
among previously obese adults with markedly reduced ANS
activity can enhance all spectral powers, indicating that
spontaneous physical activity might induce the reversibility
International Journal of Obesity
Preventive effect of physical activity on obesity
N Nagai and T Moritani
32
of the ANS activity even in middle-aged subjects. We have
reviewed a wide range of literature concerning pediatric
obesity. To the best of our knowledge, however, a limited
number of studies have been performed to assess a
physiological effect of physical activity on the ANS during
the early stage of life. Therefore, our present and previous
studies demonstrate that regular physical activity might
influence the intensity of resting metabolic rate and cardiac
autonomic control, might prevent further obesity as well as
cardiovascular diseases through enhanced ANS activity.
In conclusion, our data suggest that obese children
showed a reduction of both the SNS and PNS activities as
compared to lean children who have similar physical activity
levels, and such autonomic reduction was related to the
amount of body fat in inactive state. The reduced ANS
activity might therefore be an etiological factor of the onset
or the development of obesity. On the other hand, regular
physical activities could contribute to enhance the overall
ANS activity in both lean and obese children. Thus, the
present study further implies that regular vigorous sports
during the childhood years might be effective in child health
promotion through prevention of further obesity as well as
accompanying metabolic disorder and cardiovascular malfunction.
Acknowledgements
We are grateful to the children of the Misaki and Ikaruga
elementary schools and their families for their participation
during the experiments. We also wish to express our
appreciation to the teachers in the Misaki and Ikaruga
elementary schools for their kind support and great efforts.
This study was supported in part by the Japanese Ministry of
Education, Science, Sports, and Culture Grant-in-Aid for
Scientific Research (B) 11480011.
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