See Corresponding Editorial by Hirsch and Mackintosh on pages 2– 4 Autonomic Nervous System Activity and
the State and Development of Obesity
in Japanese School Children

Narumi Nagai,* Tamaki Matsumoto,† Hiroko Kita,‡ and Toshio Moritani* Abstract
Results: The obese children demonstrated a significantly
lower TP (6.77 Ϯ 0.12 vs. 7.11 Ϯ 0.04 ln ms2, p Ͻ 0.05), KITA, AND TOSHIO MORITANI. Autonomic nervous LF power (6.16 Ϯ 0.12 vs. 6.42 Ϯ 0.05 ln ms2, p Ͻ 0.05), system activity and the state and development of obesity in and HF power (5.84 Ϯ 0.15 vs. 6.34 Ϯ 0.07 ln ms2, p Ͻ Japanese school children. Obes Res. 2003;11:25–32.
0.01) compared with the non-obese children. A partial cor- Objective: The autonomic nervous system (ANS) plays an
relation analysis revealed that the LF and HF powers among important role in regulating energy expenditure and body 42 obese children were negatively associated with the du- fat content; however, the extent to which the ANS con- ration of obesity independent of age (LF: partial r ϭ Ϫ0.55, tributes to pediatric obesity remains inconclusive. The aim p Ͻ 0.001; HF: partial r ϭ Ϫ0.40, p Ͻ 0.01). The obese of this study was to evaluate whether sympathetic and/or children were further subdivided into two groups based on the parasympathetic nerve activities were altered in an the length of their obesity. All three spectral powers were obese pediatric population. We further examined a physio- significantly reduced in the obese group with obesity of logical association between the duration of obesity and Ͼ3 years (n ϭ 18) compared to the group with obesity the sympatho-vagal activities to scrutinize the nature of ANS alteration as a possible etiologic factor of childhood Discussion: Our data indicate that obese children possess
reduced sympathetic as well as parasympathetic nerve ac- Research Methods and Procedures: Forty-two obese and
tivities. Such autonomic depression, which is associated 42 non-obese healthy sedentary school children were care- with the duration of obesity, could be a physiological factor fully selected from 1080 participants initially recruited to promoting the state and development of obesity. These this study. The two groups were matched in age, gender, and findings further imply that preventing and treating obesity height. The clinical records of physical characteristics and beginning in the childhood years could be an urgent andcrucial pediatric public health issue.
development of the obese children were retrospectivelyreviewed to investigate the onset and progression of obesity.
Key words: childhood obesity, duration of obesity, sym-
The ANS activities were assessed during a resting condition pathetic nervous system, parasympathetic nervous sys-
by means of heart rate variability power spectral analysis, tem, heart rate variability
which enables us to identify separate frequency compo-nents, i.e., total power (TP), low-frequency (LF) power, andhigh-frequency (HF) power. The spectral powers were thenlogarithmically transformed for statistical testing.
An increase in obesity prevalence has been observed internationally in children from preschool age to adoles- cence (1). Alarming findings are now emerging from Asian Accepted for publication in final form September 3, 2002.
countries that are rapidly westernizing their lifestyles, par- *Laboratory of Applied Physiology, Graduate School of Human and Environmental Studies,Kyoto University, Kyoto, Japan; †International Buddhist University, Osaka, Japan; and ticularly their behavioral and dietary habits. As for Japan, ‡Division of Environmental Health, Hyogo Prefecture Institute of Public Health, Hyogo, the 2000 annual report of the health and physical develop- ment of the pediatric population disclosed that the number Address correspondence to Dr. Toshio Moritani, Laboratory of Applied Physiology, Grad-uate School of Human and Environmental Studies, Kyoto University, Sakyo-ku, Kyoto of obese children ages 6 to 11 years has approximately doubled over the last 20 years (2). Data from previous E-mail: 2003 NAASO studies provide strong evidence that a higher level of body OBESITY RESEARCH Vol. 11 No. 1 January 2003 Autonomic Nervous System Activity, Nagai et al.
mass index (BMI)1 during childhood can predict overweight spectral analysis have shown that obese young women later in life (3,4). To make matters worse, obesity in chil- possess significantly lower SNS activity against various dren is associated with various adverse biochemical, phys- thermogenic perturbations, such as cold exposure (23), cap- iological, and psychological effects, many of which have saicin-containing yellow curry diet (24), and mixed food strong links with chronic disease risk factors in adulthood intake (25). Unlike invasive measurements such as plasma (4,5). Thus, finding etiologic factors of obesity, as well as catecholamine concentration, catecholamine turnover, and preventing the obesity epidemic beginning in the childhood muscle sympathetic nerve activity, the HRV power spec- years, is currently a critical issue in the pediatric public tral analysis lightens the burden imposed on subjects during an experiment and is a suitable and valuable approach to Although many environmental and genetic factors are evaluating ANS activity in large-scale pediatric obesity intermingled, the development of obesity is ultimately caused by a sequential alteration of energy balance, with Accordingly, in this study, we evaluated resting ANS energy intake exceeding energy expenditure (6). The stabil- activity by means of the HRV power spectral analysis in ity of a human’s internal environment depends largely on healthy sedentary non-obese and obese school children who the orchestrations of the autonomic nervous system (ANS).
were carefully selected to avoid the physiological heteroge- Because the sympathetic branch of the system particularly neity of obesity, and investigated whether the SNS and/or contributes to coordinating energy homeostasis, the alter- the PNS activities were altered in an obese pediatric popu- ation of sympathetic nervous system (SNS) activity is lation. We also retrospectively reviewed clinical records of widely assumed to promote onset and development of obe- physical characteristics and development within the obese sity. The MONA LISA hypothesis, an acronym for Most children, and examined a physiological association between Obesities kNown Are Low In Sympathetic Activity (7), has the history of obesity (the onset and progression of obesity) been supported (8,9). However, disagreement still exists and the sympathovagal activities in order to further scruti- over the nature of the sympathetic abnormality within the nize the nature of ANS alteration as a possible etiologic adult obese population (10,11). Less research has been done with children, and the findings regarding the physiologicalrole of the SNS on pediatric obesity have been thus farinconclusive (12–14). The discrepancy is thought to arise Research Methods and Procedures
largely from the difficulty in controlling the array of vari- Subjects
ables (including age, gender, the history of obesity, other One thousand eighty obese and non-obese healthy Japa- medical complications, dietary and behavioral habits, nese children, ages 6 to 12 years, initially volunteered to physical activity levels, and emotional stress) and in ade- participate in this research. The study protocol was ap- quately assessing SNS activity in human subjects of all age proved by the Institutional Review Board of Kyoto Univer- sity Graduate School. All children and their parents were Heart rate variability (HRV) power spectral analysis is a carefully instructed about the study and gave their written well-accepted, useful, and noninvasive method, and has informed consent to participate in the study. Before obtain- provided a comprehensive quantitative and qualitative eval- ing any data from the children, the parents completed a uation of neuroautonomic function under various research standardized health questionnaire regarding their children’s and clinical settings (15–17). In general, power spectral past medical history, current health condition, past records analysis of HRV has shown at least two distinct regions of of height and body weight for estimating the history of periodicity in electrocardiogram (ECG) R-R intervals. The obesity, diet, physical activity, and lifestyle.
high-frequency component (Ͼ0.15 Hz) is a major contrib- After measuring height and body weight, percentage of utor to reflecting parasympathetic nervous system (PNS) body fat was determined by means of a bioelectrical imped- activity, and the low-frequency component (Ͻ0.15 Hz) is ance analyzer (Model TBF-534; Tanita Corp., Tokyo, Ja- associated with both SNS and the PNS activities (18,19).
pan). The analyzer has been used in several pediatric inves- Previous investigations have demonstrated that the percent- tigations because it produces a reasonable estimate for body age of body fat (20), changes in body weight and energy fat content in children (26,27). BMI was also calculated as storage (21), and glucose-induced thermogenesis (22) were body weight divided by square height. “Obesity” was de- correlated with differences in the power spectral compo- fined based on the criterion previously used in pediatric nents. A series of our recent studies with the HRV power research (Ͼ120% of the standard body weight for Japanesechildren) (3).
The results of the health questionnaires and the body 1 Nonstandard abbreviations: BMI, body mass index; ANS, autonomic nervous system; composition measurements were carefully examined. Then, SNS, sympathetic nervous system; HRV, heart rate variability; ECG, electrocardiogram; 42 obese and 42 non-obese children were selected for PNS, parasympathetic nervous system; TP, total power; LF, low frequency; HF, highfrequency; MSNA, muscle sympathetic nerve activity.
investigation of a physiological association of childhood OBESITY RESEARCH Vol. 11 No. 1 January 2003 Autonomic Nervous System Activity, Nagai et al.
R-R Spectral Analysis Procedure
Table 1. Physical characteristics of children
Our R-R interval power spectral analysis procedures have been fully described elsewhere (16,30,31). Briefly, analog Non-obese
output of the ECG monitor (MEG-6100; Nihon Kohden, (n ؍ 42)
(n ؍ 42)
Tokyo, Japan) was digitized through a 13-bit analog-to- digital converter (HTB 410; Trans Era, South Orem, UT) ata 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 se- quentially 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 (32) and displayed on a computer screenfor visual inspection. Then, the direct current component Values are expressed as means Ϯ SE.
and linear trend were completely eliminated by digital fil- tering for the band-pass between 0.03 and 0.5 Hz. The rootmean square value of the R-R interval was calculated asrepresenting the average amplitude. After passing throughthe Hamming-type data window, power spectral analysis by obesity and ANS activity. The two groups were matched in means of a fast Fourier transform was performed on a age, gender, and height. All children were in good health consecutive 256-s time series of R-R interval data obtained and had no personal or family history of hypertension, cardiovascular disease, diabetes mellitus, or other endocrine Based on our previous investigations (16,30,31,33), the diseases. None of the children were taking any medications.
spectral powers in frequency domain were quantified by According to the nutritional survey included in the health integrating the areas under the curves for the following questionnaire, daily energy intake and nutritional content of respective band width: the low-frequency (LF: 0.03 and food did not significantly differ between the two groups.
0.15 Hz), an indicator of both SNS and PNS activity; the Concerning the physical activity level, none of the children high-frequency (HF: 0.15 and 0.5 Hz), which solely reflects in these groups regularly engaged in sports activities or the PNS activity; and the total power (TP: 0.03 and 0.5 Hz), aerobic exercises. The descriptive characteristics of the chil- representing the overall ANS activity. Because basal spec- tral absolute values differed greatly among individuals, thespectral powers were then logarithmically transformed for Methods
The children came at 8:30 AM to the temporary laboratory that was set up in the school infirmary. All experiments Statistical Analyses
were performed in the morning, and the entire research All data are expressed as mean Ϯ SE. Student’s unpaired project lasted for 2 consecutive days in June. The room t test was performed to assess statistical differences in was temperature controlled (25 °C), quiet, and comfortable, physical characteristics and the parameters of the ANS with minimal arousal stimuli. After appropriate skin prep- activity between the obese and non-obese groups. Partial aration, the subjects were fitted with ECG electrodes and correlation analysis was performed to examine the re- then rested for at least 15 minutes before the start of the lationships between the ANS parameters and the dura- tion of obesity independently of a covariate, i.e., age. All p After the resting period, the CM lead ECG signals were values were two-sided. A p value of Ͻ0.05 was chosen as continuously recorded for 4.5 minutes while each child the level of significance. All statistical analyses were made remained seated in a chair and breathed normally (28). It on a personal computer with a commercial software should be noted that, according to our preliminary experi- package (SPSS version 10.0J for Windows; SPSS Inc., ment as well as accepted parameters of pediatric physiology (29), children’s breathing frequency is generally higher than9 rates per minute (Ͼ0.15 Hz). Thus, we assumed that,without controlling the respiration rates during the ECG measurements, respiratory-linked variations in heart rate did Figure 1 represents typical sets of raw R-R intervals and not overlap with low-frequency heart rate fluctuations the power spectral data obtained from an obese and a non-obese child, respectively, during the resting condition.
OBESITY RESEARCH Vol. 11 No. 1 January 2003 Autonomic Nervous System Activity, Nagai et al.
Figure 1: Examples of ECG R-R interval changes and the corresponding power spectra for an obese and a non-obese child at rest,respectively.
According to visual inspection, the obese child possessed HF: partial r ϭ Ϫ0.40, p Ͻ 0.01). A statistical analysis remarkably reduced ranges in R-R variability, as well as in demonstrated that all three spectral powers were signifi- both frequency components of the power spectrum, com- cantly reduced in the group with obesity of Ͼ3 years (n ϭ 18) compared to the group with obesity of Ͻ3 years The statistical analysis revealed that there were signifi- (n ϭ 24; TP: 6.35 Ϯ 0.15 vs. 7.33 Ϯ 0.09 ln ms2, p Ͻ 0.01; cant differences in the R-R spectral parameters between the LF: 5.78 Ϯ 0.15 vs. 6.67 Ϯ 0.12 ln ms2, p Ͻ 0.01; HF: two groups. The obese group had a significantly higher 5.37 Ϯ 0.20 vs. 6.46 Ϯ 0.13 ln ms2, p Ͻ 0.01).
resting heart rate compared with the non-obese group(90.7 Ϯ 1.5 vs. 84.3 Ϯ 1.0 beats per minute, p Ͻ 0.001). AsFigure 2 demonstrates, all the spectral powers were signif- Discussion
icantly lower in the obese group than in the non-obese group This study provides valuable information regarding a (TP: 6.77 Ϯ 0.12 vs. 7.11 Ϯ 0.04 ln ms2, p Ͻ 0.05; LF: potential etiologic association between childhood obesity 6.16 Ϯ 0.12 vs. 6.42 Ϯ 0.05 ln ms2, p Ͻ 0.05; HF: 5.84 Ϯ and ANS activity. The main findings are that healthy sed- 0.15 vs. 6.34 Ϯ 0.07 ln ms2, p Ͻ 0.01), indicating that both entary obese school children possess much lower sympa- SNS and PNS activity decrease in obese children.
thetic and parasympathetic nerve activities. In addition, a To further investigate an association between the HRV degree of these autonomic reductions depends on the dura- spectral powers and the history of obesity, the obese chil- tion of obesity independent of a subject’s age.
dren were subdivided into two groups based on the length of It is well known that the coordination of energy ho- obesity. It has been shown that physiological factors such as meostasis particularly relies on the normal functioning of age influence HRV (34,35); thus, we performed the partial the sympathoadrenal system. As the MONA LISA hypoth- correlation analysis to examine the relationship after adjust- esis indicates (7), it is reasonable to assume that reduced ment for age. As Figure 3 shows, the LF and HF powers SNS activity leads to a lower rate of thermogenesis, and among 42 obese children were negatively correlated with consequently, to a positive energy balance and obesity.
the duration of obesity (LF: partial r ϭ Ϫ0.55, p Ͻ 0.001, Despite intensive research, physiological roles of SNS ac- OBESITY RESEARCH Vol. 11 No. 1 January 2003 Autonomic Nervous System Activity, Nagai et al.
Figure 2: Comparison of total, low-frequency, and high-frequency powers between the obese and the non-obese groups, respectively.
Results are expressed as mean Ϯ SE for each group. *p Ͻ 0.05, **p Ͻ 0.01.
tivity on human obesity remain unclear. The different meth- results over the nature of the SNS affected by obesity (36).
odologies used among investigators may have caused this Technical developments have allowed direct intraneural re- situation. For instance, plasma and urinary norepinephrine cordings of sympathetic nerve traffic by microneurography, estimates, both of which are commonly used as global but the technique is limited to peripherally measuring SNS indexes for sympathetic activity, have provided conflicting activity in the skin and skeletal muscles (9,37). The muscle Figure 3: Partial correlations between both the low-frequency and the high-frequency powers and the duration of obesity, independent ofa physiological effect of age among 42 obese children.
OBESITY RESEARCH Vol. 11 No. 1 January 2003 Autonomic Nervous System Activity, Nagai et al.
sympathetic nerve activity (MSNA) has been applied to ues of spectral components to examine the ANS features of obesity research, generally demonstrating a positive corre- pediatric obesity, and provided the evidence that the TP, LF, lation between the amount of body fat and MSNA (10,11).
and HF powers were all more substantially reduced in the Because measuring MSNA requires the insertion of a fine obese than in the non-obese children. It has been pointed out tungsten microelectrode and because MSNA is mainly re- that the frequency component of HRV spectral analysis, lated to the control of blood pressure rather than energy which reflects only the SNS activity, is difficult to single metabolism, the methodology is not relevant to investigat- out. The normalized units and the ratios, i.e., LF/HF, have ing SNS activity, especially in a pediatric and epide- been used as alternative indexes to evaluate SNS and PNS activities (13,16,22). These indexes have been valuable The spectral analysis of HRV has attracted considerable and applicable to clinical settings as well as basic physio- attention from investigators in various physiological fields, logical research, but the results could overestimate or including diabetes and obesity research both for adult (16, underestimate the sympatho-vagal activity because the in- 20 –22, 31) and pediatric populations (13,14,38 – 41), and dexes are relative values. As described above, neuro- has become a reliable noninvasive measure to appraise physiological contributions to the LF and HF powers have ANS activity. As to an association of the ANS and energy been clarified, and SNS activity, at least in part, does homeostasis, Landsberg and Young (42) indicated that cat- contribute to the LF power even in the resting condition echolamine turnover within cardiac tissue could precisely (23). We recognize that the LF power, like all other indi- reflect autonomic events that affect energy metabolism else- cators, has its limitations in precisely measuring SNS ac- where in the body. We have conducted a pharmacological tivity. Nevertheless, under the condition that the LF power blockade experiment to confirm the validity of the HRV together with the HF power and the TP all significantly power spectral analysis for evaluating and quantifying the decrease, which has appeared in presently healthy obese sympathovagal activity. In short, after atropine, a parasym- children, it is plausible to assume that both SNS and PNS pathetic muscarinic antagonist, was intravenously injected, R-R variability was markedly reduced and the HF compo- Even during childhood, low levels of PNS activity are nents were almost entirely abolished, whereas the LF com- associated with cardiac autonomic neuropathy in diabetics ponents were partly decreased. When propranolol, a ␤-ad- with poor metabolic control (39), duration of diabetes (40), renoceptor antagonist, was additionally injected, heart rate and elevated blood pressure (47). Taking the previous re- fluctuations were almost entirely abolished, and the resting sults into consideration, reduced PNS activity appearing in energy expenditure was significantly reduced (23,25,31).
presently healthy obese children might be a conceivable Previous clinical studies further demonstrated that noninsu- early sign to predict cardiovascular and metabolic health. As lin-dependent diabetes mellitus patients with neuropathy to the SNS activity, our results suggest the possibility that had markedly reduced R-R interval fluctuations and HRV the MONA LISA hypothesis, indicating that obesity is spectral power at rest compared with healthy individuals associated with a relative or absolute reduction in the ther- (16,30). These findings support the previous studies (18,19) mogenic component of SNS activity, might, at least in part, and indicate that 1) the HF power is associated solely with contribute to our understanding of the pathophysiological PNS activity, and the LF power is jointly mediated by PNS features of pediatric obesity. Normal or increased levels of and SNS activities, and 2) R-R interval variability and the SNS activity and its blunted responsiveness seem to be integrated values of all the components of power spectra present in adult-established obesity (9,11,23–25). Taken could reflect the overall ANS activity. Concerning the ex- together, the nature of SNS alteration in human obesity perimental setting, several studies have faced a difficulty in might diversify depending on the time in which the obese using HRV spectral analysis during nonresting conditions state occurs, is promoted, or is established.
such as dynamic exercise, but the validity of spectral anal- We have extensively reviewed the literature regarding ysis of HRV under the resting condition, which we used in pediatric obesity. To the best of our knowledge, however, a this study, has been well documented (16,17,43). Therefore, limited number of studies have been conducted to examine the application of HRV spectral analysis in a childhood the physiological role of ANS in human obesity during the population has distinct advantages over the existing meth- early stage of life. Martini et al. (13) and Riva et al. (14) ods for autonomic function in that it is noninvasive, less used time- and frequency-domain of HRV measured by time consuming, and less upsetting for young participants 24-hour Holter recordings, and suggested that obese ado- lescents with metabolic changes, such as hyperinsulinemia, Although quantification and interpretation of HRV re- euglycemia, or dislipidemia, may have a sympathovagal main a complex issue (15,44), the efficacy and applicability balance, characterized by a primary decrease in PNS activ- of the technique used in the present investigation have been ity with a relative prevalence of SNS activity. Yakinci et al.
shown in previous research (16,30,31,33,45,46). By apply- (12) performed noninvasive autonomic tests, including or- ing this analysis procedure, we measured the absolute val- thostatic test, Valsalva maneuver, and deep breathing, and OBESITY RESEARCH Vol. 11 No. 1 January 2003 Autonomic Nervous System Activity, Nagai et al.
indicated normal activity of SNS and hypoactivity of PNS fare Center of Ako and Tatsuno in Hyogo Prefecture for in obese children. According to the study of Wawryk et al.
their cooperation and assistance during the experiments.
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