Background
Metabolic syndrome, also known as insulin resistance syndrome or syndrome X, is the term most commonly used to identify a constellation of metabolic disorders [
1]. In 2001, the National Cholesterol Education Program’s Adult Treatment Panel III (NCEP: ATP III) defined metabolic syndrome as having three of the five following components: glucose intolerance, hypertension, insulin resistance, abdominal obesity, and dyslipidemia [
2]. Metabolic syndrome is associated with an increased risk of type 2 diabetes [
3‐
5] and cardiovascular disease (CVD) [
4,
6].
Over the last few decades, the prevalence of metabolic syndrome has increased worldwide, and it has become a major public health concern in many countries, including several Asian countries [
7‐
9]. According to data from the Korean National Health and Nutrition Examination Survey (KNHANES, 1998–2007), the age-adjusted prevalence of metabolic syndrome among Korean adults rapidly increased from 24.9% in 1998 to 31.3% in 2007 [
9]. The rise in the prevalence of metabolic syndrome was related to both an increased prevalence of obesity [
10,
11] and decreased physical activity levels [
12‐
14].
A low level of cardiorespiratory fitness (CRF) is a major contributing risk factor for metabolic syndrome [
15‐
17], as well as a predictor of overall mortality [
18‐
22]. Other studies showed that a high level of CRF is associated with a significantly reduced incidence of metabolic syndrome [
15,
23‐
25]. Thus, maintaining and improving CRF is an important strategy for the prevention of metabolic syndrome.
While several studies have indicated that increased CRF and decreased BMI reduced the risk of metabolic syndrome [
15,
24] the current study is one of the first studies to explore the combined association of BMI and CRF with the prevalence of metabolic syndrome in Korean adults. Most previous studies have used maximal oxygen consumption (VO2 max) to measure CRF, which has been the gold standard measurement for CRF [
26]. However, this method is challenging due to the high cost of the equipment required and the need for trained personnel. For this reason, heart rate during or after submaximal exercise has been used as an alternative method to measure CRF in large epidemiological studies [
24,
27,
28]. Furthermore, the step test has been proven to be safe and inexpensive, and therefore can be used in the clinic for patients with a history of cardiac events, as well as in situations where the equipment needed to perform the VO2 max test is not available.
Therefore, the purpose of this study was to analyze the association between CRF, measured by heart rate recovery (HRR) after the step test, and the prevalence of metabolic syndrome in Korean adults. We further analyzed the combined association of BMI and CRF with the prevalence of metabolic syndrome.
Discussion
Reductions in physical activity and CRF are associated with increased prevalence and incidence of metabolic syndrome. In our study, we found that a lower level of CRF, as indicated by slower HRR following exercise, was associated with increased prevalence of metabolic syndrome in Korean men. A low level of CRF is a known risk factor for both cardiovascular disease and type 2 diabetes; however, the importance of the current study is the use of HRR after submaximal exercise as a measure of CRF. A prior study has validated the Tecumseh step test as an appropriate measurement to indicate cardiorespiratory fitness [
34]. In comparison to the other more elaborate and expensive test approaches previously used to obtain VO2 max, the Tecumseh step test, used in the present study, is a relatively quick and easy method that can be used in most epidemiological and clinical settings [
34]. Findings from the current study also indicate that the association between CRF and the prevalence of metabolic syndrome was somewhat gender dependent, although this relationship was less clear when the combined association of BMI and CRF with metabolic syndrome prevalence was examined.
The main finding of this study is the significant association between faster HRR after submaximal exercise and the lower prevalence of metabolic syndrome in men, suggesting that fitter men participants are at lower risk of metabolic syndrome. The association between CRF and metabolic syndrome has been reported previously. Laaksonen et al. [
17] reported a significant inverse association between CRF and prevalence of metabolic syndrome even after adjustment for major confounders. In addition, Lamonte et al. [
15] reported that the incidence of metabolic syndrome was significantly reduced among fit individuals (OR: 0.47, 95% CI: 0.40 to 0.54) compared with the least fit individuals (lower tertile). The current study and previously reported studies suggest that fitter individuals are less likely to develop metabolic syndrome compared with those who are unfit. However, physical fitness is not the only contributor for the development of metabolic syndrome.
There are other factors independent of CRF that influence the development of metabolic syndrome. In our study, approximately 50% of obese individuals had metabolic syndrome. Similarly, several previous studies found that the components of metabolic syndrome were closely associated with obesity [
10]. In a prospective cohort study, Katzmarzyk et al. [
35] reported that overweight men were 4.5 times (95% CI: 4.2-5.3) more likely to develop metabolic syndrome, and obese men were 30.6 times (95% CI: 26.7-35.0) more likely to develop metabolic syndrome. It is not surprising that more obese individuals have a higher prevalence of metabolic syndrome; one of the five metabolic syndrome components directly reflects degree of adiposity. In our study, we also confirmed that more obese individuals are more likely to have metabolic syndrome.
To further understand the combined association of obesity and CRF with the prevalence of metabolic syndrome, we have stratified our participants into nine groups according to their BMI and fitness levels. Compared with those who had low BMI and high CRF, those with high BMI and low CRF were 18.8 and 8.1 times more likely to have metabolic syndrome in men and women, respectively. It is noteworthy that among those with high BMI, fitter individuals of either gender have a lower risk of metabolic syndrome, suggesting the importance of fitness in the development of metabolic syndrome in Korean adults. For this study, CRF was indicated by the HRR measurement taken after administering the Tecumseh step test. Previous epidemiological studies have typically used the graded treadmill test or the VO2 max to measure CRF, when investigating the association between CRF and health-related outcomes. However, administering the VO
2 max test requires specialized and expensive equipment, in addition to requiring well-trained technicians [
34]. Recent studies indicate that CRF can more conveniently be assessed by measuring HRR after treadmill exercise. This HRR approach combined with treadmill exercise is a safe and inexpensive method, and has been proven to be valid [
34‐
36]. An additional benefit from using the HRR approach lies in its demonstrated value in treating key components of metabolic syndrome, to include positive outcomes for fasting plasma glucose [
37], HDL cholesterol [
38‐
40], and insulin levels [
41], and prevalence of type 2 diabetes mellitus [
42]. Therefore, based on the findings from these studies [
37‐
42], and supported by previously reported studies, we conclude that HRR following exercise is a safe and feasible method for estimating CRF in an epidemiological setting [
28].
In our study, we have observed gender differences in the association of BMI and CRF with the components of metabolic syndrome. CRF was significantly associated with fasting glucose and HbA1c in men only, while BMI was significantly associated with fasting glucose and HbA1c in women only. The discrepancies found between genders could be due to the gender-specific distribution of adiposity and level of physical activity. Kriska et al. [
36] reported that physical activity and physical fitness were associated with fasting glucose levels in men, but not in women. Authors speculated the reason for this gender difference was due to lower levels of physical activity in women participants. Indeed, in our previously reported study with the same cohort, we found significantly lower vigorous, moderate, and total physical activity levels in women participants compared with men [
14]. Another explanation for the gender differences observed in our study could be the distribution of adiposity. Waist circumference and BMI were significantly lower among women participants compared with men participants in our study. Meanwhile, our women participants with high BMI still had significantly increased metabolic risk factors. The gender differences observed in our study require further investigation.
In understanding the mechanism of association between HRR and the prevalence of metabolic syndrome, independent and dependent of adiposity, it is necessary to understand the impact of parasympathetic and sympathetic nervous system activity on heart rate. The changes in cardiovascular function associated with low-intensity exercise are primarily mediated by parasympathetic withdrawal, and, as exercise intensity increases, additional cardiovascular reactivity is mediated by increased sympathetic outflow [
37]. The fall in heart rate immediately after exercise is considered to be a function of the reactivation of the parasympathetic nervous system [
38]. Delayed HRR after exercise could be related to attenuated parasympathetic reactivity, which has been described as a marker of decreased vagal activity [
39]. Attenuated HRR induced by decreased vagal activity is a powerful risk factor for all-cause mortality [
39‐
43].
The current study has several limitations. First, the level of HRR from the Tecumseh step test might be affected by BMI. The high BMI group could have an increase in heart rate that is greater than those of the other groups when they step up and down. Despite this limitation, this step test has been frequently used in clinical settings as a representative CRF test [
44‐
46]. Second, due to the cross-sectional nature of this study, it was not possible to control some confounding factors as their diet and medications that may have affected the results. Factors that could have produced confounding influences included that the participants were recruited in this study by using convenience sampling, a relatively small sample size was used, and the limited age range for the group (middle age). Because of these biases and limitations, it is difficult to maintain that the findings of the present study accurately represent the Korean population in general.
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Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
JJ conceived and designed the study. HSH and LJA conducted the data analyses and drafted the manuscript. JJ led the drafting of manuscript and prepared the final version. All authors revised the manuscript for important content and have read and approved the final version.