Metabolic syndrome is a condition linking insulin resistance, dyslipidemia, hyperglycemia, and hypertension (7) that increases the risk of developing diabetes (18,24), cardiovascular disease (20,25), and subsequent cardiovascular morbidity and mortality (8). Therefore, it is an early marker of increased risk of atherosclerosis and its associated complications. Metabolic syndrome was prevalent in 21.8% of people age 20 yr or older in the Third National Health and Nutrition Examination Survey (NHANES) obtained between 1988 and 1994 (12), which increased to 34.3% in the 2003–2006 NHANES observation (13). The prevalence of overweight children and adolescents in the NHANES study increased from 5% between 1976 and 1980 to 15% between 1999 and 2000 (30). Thus, it is not surprising that metabolic syndrome is now becoming prevalent in children and adolescents (6), placing them at heightened cardiovascular risk at very young age. The International Diabetes Federation recently recommended definitions for each component of metabolic syndrome in children and adolescents, consisting of having abdominal obesity plus at least two of the other four components: hypertriglyceridemia, low HDL cholesterol, hyperglycemia, and hypertension (39). Because abdominal obesity is the hallmark measure of metabolic syndrome, the role that physical activity may have in altering visceral adiposity and metabolic syndrome is apparent (33).
Regular physical activity in prospective observational studies is one lifestyle modification that can favorably affect cardiovascular health outcomes, including cardiovascular disease, thromboembolic stroke, hypertension, type 2 diabetes mellitus, and obesity (23). As such, it is recommended that to promote and maintain health, all healthy adults between 18 and 65 yr need moderate intensity physical activity for a minimum of 30 min on 5 d each week (14,19). For children and adolescents between 5 and 17 yr, it is recommended that moderate intensity physical activity should be accumulated for at least 60 min·d−1, although some health benefits may occur with at least 30 min·d−1 (21,37). As described in a systematic review (21), it is not clear whether physical activity lessens the risk of developing metabolic syndrome in children and adolescents. Two studies that used self-reported measures of physical activity found weak or modest associations with metabolic syndrome (22,32), whereas other studies that used objective measures from accelerometers found significant and stronger associations (2,4). However, the pattern of physical activity in terms of both volume and intensity on individual components of metabolic syndrome has not been studied in children and adolescents. This information is important for physical activity recommendations to lessen the risk of developing metabolic syndrome and its components.
We have used a step activity monitor to quantify not only the total amount of daily ambulation but also the cadence of daily ambulation, which serves as a measure of intensity (5,16,17). The purposes of this study were 1) to compare daily ambulatory measures in children, adolescents, and young adults with and without metabolic syndrome, and 2) to assess which metabolic syndrome components, demographic measures, and body composition measures are associated with daily ambulatory measures. We hypothesize that objectively measured daily ambulatory cadences are lower in subjects with metabolic syndrome, particularly in those with higher values of body fat percentage.
METHODS
Subjects
Institutional review board approval, informed consent, and child’s assent
The procedures used in this study were approved by the institutional review board at the University of Oklahoma Health Sciences Center. For subjects younger than 18 yr, both the child and the parent or legal representative agreed to participate by signing the child’s assent form. Subjects 18 yr and older signed the informed consent form.
Recruitment
A total of 250 healthy subjects between 10 and 30 yr participated at the General Clinical Research Center and the Children’s Medical Research Institute Diabetes and Metabolic Research Program from September 2006 to November 2009. The subjects were recruited by local newspaper advertisements, university e-mail advertisements, and informational flyers distributed in Oklahoma City and surrounding areas.
Medical screening through history, physical examination, and anthropometry
Subjects were evaluated during a medical history and physical examination. Demographic information, pubertal status by Tanner stage, height, weight, body mass index, cardiovascular risk factors, comorbid conditions, blood samples, and a list of current medications were obtained. Waist and hip circumferences were measured and recorded to the nearest millimeter by trained technicians using a plastic measuring tape (11,36).
Inclusion and exclusion criteria
Subjects were included in this study if they met the following criteria: (a) between 10 and 30 yr, (b) a Tanner stage of 2 or greater for boys and girls, and (c) subjects were ambulatory. Subjects were excluded for the following criteria: (a) under treatment for hypertension, (b) under treatment for dyslipidemia, (c) current smoking, (d) insulin- or noninsulin-dependent diabetes mellitus, (e) use of oral contraceptives, and (f) history of any form of cardiovascular disease, pulmonary disease, renal disease, liver disease, or active cancer.
Metabolic syndrome groups
According to the Inter-national Diabetes Federation (7,39), metabolic syndrome in children and adolescents is defined as having abdominal obesity plus at least two of the other four components of metabolic syndrome consisting of elevated triglycerides, reduced HDL cholesterol, elevated blood pressure, and elevated fasting glucose. Abdominal obesity in children and adolescents between 10 and 15 yr was defined as a waist circumference value ≥90th percentile of age, sex, and ethnicity norms or the adult cutoff point, whichever is lower. For subjects 16 yr and older, the adult criteria was used to define abdominal obesity, consisting of a waist circumference of ≥94 cm for men and ≥80 cm for women. Of the remaining four components of metabolic syndrome, the adult definitions of elevated triglycerides (>150 mg·dL−1), elevated blood pressure (>130/85 mm Hg), and elevated fasting glucose (>100 mg·dL−1) were used. Reduced HDL cholesterol in children and adolescents between 10 and 15 yr was defined as a value <40 mg·dL−1, whereas in those 16 yr and older, the adult criteria of <40 mg·dL−1 in men and <50 mg·dL−1 in women was used. Of the 250 subjects included in this study, 45 (18%) screened positive for metabolic syndrome, whereas the remaining 205 (82%) screened negative.
Measurements
Ambulatory activity monitoring. Instrumentation and procedures
Daily ambulatory strides, durations, and cadences were assessed using a step activity monitor (Step Watch 3; Orthocare Innovations, Oklahoma City, OK) as previously described (15). Ambulatory activity was measured during seven consecutive days in which subjects were instructed to wear the monitor during waking hours and to remove it before retiring to bed. The step activity monitor was attached to the right ankle above the lateral malleolus using elastic Velcro straps and continuously recorded the number of steps taken on a minute-to-minute basis. The accuracy of the step activity monitor exceeds 99% ± 1% in older adults (15) as well as in children (27).
Variables obtained from the step activity monitor
The step activity monitor records the number of ambulatory strides taken per minute for each minute throughout a 24-h period. After downloading data from the step activity monitor to a computer, the software program displays the number of strides taken and the number of minutes spent ambulating each day, from which a daily average cadence is calculated. Any minute in which ambulation occurred (i.e., at least one stride was recorded) was defined as an active minute, and the total number of strides were divided by the total number of active minutes to yield an average cadence of ambulation. The daily ambulatory strides and time are further analyzed by the software program and are quantified into the following variables: maximum cadence for 60, 30, 20, and 5 continuous minutes of ambulation each day, maximum cadence for 1 min of ambulation each day (i.e., the minute having the single highest cadence value each day), and peak ambulatory index obtained by ranking all minutes of the day according to cadence and then taking the highest 30 values. All of these outcome measures are recorded for each day, and then the daily values are averaged for the 7-d monitoring period. In apparently healthy subjects, the test–retest intraclass reliability coefficient for the measurement of total daily strides and total daily minutes of activity for the 7-d period are R = 0.94 and R = 0.91, respectively (15). The intraclass reliability coefficients for the remaining variables pertaining to daily ambulatory cadences range from R = 0.83 to R = 0.94 (15).
Body composition assessment
After an overnight fast of at least 8 h, body fat percentage, fat mass, and fat-free mass were obtained using a BC-418 eight-electrode bioelectrical impedance analysis device (Tanita Corp., Tokyo, Japan) (28,31,34). Subjects stood barefoot on the base of the unit, which has two stainless steel rectangular foot-pad electrodes fastened to a metal platform set on force transducers. During this measurement, subjects held hand-grip electrodes. The system has a total of eight electrodes, two for each hand and foot. All electrodes are connected to a digital circuit board. Age, height, and body type (all classified as standard and none classified as athletic) were entered for each subject for calculation of body fat percentage. The assessment of body composition through bioelectrical impedance using model BC-418 has been validated against measurements obtained from dual-energy x-ray absorptiometry in men and women ranging in age from 6 to 64 yr (31).
Statistical Analyses
An independent t-test was used to compare the means of continuous measures between the metabolic syndrome group and the control group. A single degree of freedom chi-square test was used to compare the proportions of categorical measures between the two groups. ANCOVA was used to obtain adjusted means and to examine the differences between the two groups for daily average cadence and daily strides, adjusted for each covariate individually. Multiple linear regression procedures with the pairing of metabolic syndrome status, each individual covariate and metabolic syndrome component (e.g., age, weight, elevated fasting glucose, etc.) serving as the independent variables, and daily average cadence and daily strides serving as the dependent variables were used to obtain slopes and partial R2 values. All analyses were performed using the NCSS statistical package (NCSS Inc., Kaysville, UT).
RESULTS
No significant differences were observed between the two groups for age (P = 0.437), height (P = 0.096), sex (P = 0.445), and race (P = 0.072) (Table 1). The metabolic syndrome group had higher values for body mass index (P < 0.001), waist–hip ratio (P < 0.001), body fat percentage (P < 0.001), fat mass (P < 0.001), and fat-free mass (P < 0.001). By definition, all subjects with metabolic syndrome had abdominal obesity, which was a higher prevalence than those without metabolic syndrome (P < 0.001). As expected, those with metabolic syndrome had a higher prevalence of the components of metabolic syndrome, consisting of elevated fasting glucose (P < 0.001), elevated blood pressure (P = 0.002), elevated triglycerides (P < 0.001), and reduced HDL cholesterol (P < 0.001).
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TABLE 1: Clinical characteristics of subjects with and without metabolic syndrome.
As shown in Table 2, the groups were significantly different on each measure of ambulatory activity during a 7-d monitoring period, except for the daily ambulatory time (P = 0.077). The metabolic syndrome group ambulated at a slower average cadence throughout the day (P = 0.012) and at slower cadences for continuous durations of 60 min (P = 0.006), 30 min (P = 0.005), 20 min (P = 0.003), 5 min (P = 0.002), and 1 min (P = 0.001). The metabolic syndrome group also had a slower discontinuous ambulatory cadence as measured by the peak ambulatory index (P = 0.003). The metabolic syndrome group took fewer strides per day (P < 0.001) than the controls, translating to more than 2000 fewer steps per day (8152 and 10,282 steps per day in the metabolic syndrome and control groups, respectively).
TABLE 2: Ambulatory activity of subjects with and without metabolic syndrome.
To assess which metabolic syndrome components, demographic measures, and body composition measures are associated with daily ambulatory cadence, we selected the daily average cadence for analyses because it provides an overall estimate of the rate of ambulation (Table 3). After adjustment for metabolic syndrome status, average cadence is linearly associated with age (P < 0.001), body fat percentage (P < 0.001), fat mass (P < 0.01), fat-free mass (P < 0.05), and sex (P < 0.05). The linear association between daily average cadence and body fat percentage in subjects with and without metabolic syndrome is shown in Figure 1. Average cadence remained significantly lower for the metabolic syndrome group after adjusting for age (P = 0.013), height (P = 0.008), weight (P = 0.024), waist–hip ratio (P = 0.004), fat-free mass (P = 0.002), sex (P = 0.015), race (P = 0.025), and elevated blood pressure (P = 0.005). Average cadence was no longer significantly different between the two groups after adjusting for body mass index (P = 0.155), body fat percentage (P = 0.683), fat mass (P = 0.973), elevated fasting glucose (P = 0.296), elevated triglycerides (P = 0.245), and reduced HDL cholesterol (P = 0.088).
TABLE 3: Association between daily average cadence and covariates, controlled for metabolic syndrome status, and comparison of average cadence in subjects with and without metabolic syndrome after adjustment for each covariate.
FIGURE 1: Daily average cadence versus body fat percentage in subjects with and without metabolic syndrome.
In contrast to average cadence, which is a measure of the rate of walking, the number of strides taken per day is a measure of ambulatory volume. Thus, the associations between daily ambulatory strides and metabolic syndrome components, demographic measures, and body composition measures are depicted in Table 4. After adjustment for metabolic syndrome status, daily ambulatory strides is linearly associated with body fat percentage (P < 0.05), fat mass (P < 0.05), and reduced HDL cholesterol (P < 0.05). Daily ambulatory strides remained significantly lower for the metabolic syndrome group after adjusting for age (P = 0.001), height (P = 0.002), waist–hip ratio (P = 0.001), fat-free mass (P = 0.009), sex (P = 0.001), race (P = 0.003), elevated blood pressure (P = 0.001), and elevated triglycerides (P = 0.006). Daily ambulatory strides was no longer significantly different between the two groups after adjusting for body mass index (P = 0.091), body fat percentage (P = 0.225), fat mass (P = 497), elevated fasting glucose (P = 0.060), and reduced HDL cholesterol (P = 0.069).
TABLE 4: Association between daily ambulatory strides and covariates, controlled for metabolic syndrome status, and comparison of ambulatory strides in subjects with and without metabolic syndrome after adjustment for each covariate.
DISCUSSION
Metabolic syndrome and daily ambulatory activity.
A novel finding in this study is that ambulatory cadences of continuous durations ranging from 1 min to 1 h were slower in children, adolescents, and young adults with metabolic syndrome than those without metabolic syndrome. Furthermore, the metabolic syndrome group also had slower discontinuous ambulatory cadence, as measured by the peak ambulatory index, and they took fewer ambulatory strides each day. However, the daily amount of time spent ambulating was not different between subjects with and without metabolic syndrome. According to recent normative data and recommendations, both the metabolic syndrome group and the control group fall below the expected range of 11,000 to 15,000 steps per day in children and 10,000 to 11,700 steps per day in adolescents (38). Given that the daily average cadence of the metabolic syndrome group is 13.6 strides per minute (27.2 steps per minute), those with metabolic syndrome would need to ambulate for an average of nearly two additional hours per day to achieve 11,000 steps per day. In the best-case scenario, if they were to ambulate at a cadence associated with their fastest daily minute (51.2 strides per minute or 102.4 steps per minute), the metabolic syndrome group would need to ambulate for an additional 30 min·d−1 to achieve 11,000 steps per day.
Our data suggest that children, adolescents, and young adults with metabolic syndrome engage in similar durations of ambulatory activities throughout each day compared with controls, but they do so at slower paces. The lower intensity of ambulation in the metabolic syndrome group should result in lower daily energy expenditure of physical activity, thereby favoring long-term positive energy balance, and exacerbating their greater body weight and fatness even further. Our results support the findings that the odds of having a cluster of risk factors increases with descending quartiles (4) and quintiles (2) of physical activity assessed by accelerometers. Collectively, these findings and our results support the notion that intensity of physical activity is an important factor in distinguishing between those with and without metabolic syndrome. This is further supported by studies showing that cardiorespiratory fitness is protective against developing metabolic syndrome in children and adolescents (1,3,4). It is not surprising that the association between daily physical activity and metabolic syndrome is much weaker in studies quantifying activity with questionnaires (22,32), as self-reported moderate-to-vigorous physical activity is overestimated by nearly 30 min·d−1, with the greatest errors found in the most inactive subjects (26).
Components of metabolic syndrome and daily ambulatory activity
Another key finding in this investigation is that body fatness, adjusted for metabolic syndrome status, is the most important determinant of daily ambulation in children, adolescents, and young adults. Daily ambulatory activity can be quantified in different aspects, consisting of the rate of walking (cadence), the duration of walking, and the number of strides taken while walking. We had several cadence measures to choose from to evaluate the association between the rate of walking with metabolic syndrome components, demographic measures, and body composition measures, and we selected the average cadence because it provides an overall estimate of the rate of daily ambulation. Body fat percentage and fat mass were both significantly and negatively associated with average cadence and daily ambulatory strides. Furthermore, the difference in ambulatory cadence and daily ambulatory strides between subjects with and without metabolic syndrome was no longer significant after adjusting for body fat percentage and fat mass. These results indicate that subjects with high levels of body fat ambulate at a slower pace and take fewer strides than those with less body fat, and that the lower ambulatory measures in those with metabolic syndrome is primarily due to their greater body fatness. Our findings agree with others that found a strong association between obesity and objectively measured physical activity with either a pedometer (10) or an accelerometer (9,29,35).
Age, sex, and daily ambulatory activity
It is important to note that both age and sex, adjusted for metabolic syndrome status, are associated with ambulatory cadence but not with daily ambulatory strides in children, adolescents, and young adults. However, the difference in ambulatory cadence between subjects with and without metabolic syndrome remained after adjusting for age and sex. These results indicate that ambulatory cadence is slowest in children and linearly increases up to age 30, men ambulate faster than women across this age range, and neither age nor sex eliminate the difference in ambulatory cadence between those with and without metabolic syndrome. The interpretation is that although age and sex were associated with ambulatory cadence, the metabolic syndrome groups were not different on age or sex, and therefore adjustment of these variables has minimal effect on the group difference for ambulatory cadence. For the measure of daily ambulatory strides, our finding that age and sex are not associated with strides per day disagrees with a recent review, which reports a decline in steps per day from childhood through adolescence and that boys take more steps than girls (38). The reason for this discrepancy is not clear, but our data suggest that average cadence is more closely related to demographic characteristics, such as age and sex, than daily ambulatory strides.
Limitations
There are limitations to this study. The cross-sectional research design of this study does not allow causality to be established when examining the relationship between daily ambulatory activity and metabolic syndrome, the components of metabolic syndrome, demographic measures, and body composition. Thus, it is possible that metabolic syndrome slows ambulation or that subjects who ambulate slowly are more likely to develop metabolic syndrome and the component of metabolic syndrome. A self-selection bias may also exist regarding study participation. Although we directly measured ambulatory activity, there are limitations associated with the step activity monitor. It is possible that the patients did not wear the step activity monitor during portions of their waking hours, thereby resulting in an underestimate of daily ambulation. We believe this possibility is unlikely because long durations in which no active minutes were recorded during daytime hours were rarely evident from the software graphs. Three subjects in the control group and one subject in the metabolic syndrome group had 1 d with zero steps recorded until late afternoon. In these cases, each of the 4 d was excluded from the monitoring period, and the subjects were asked to wear the monitor for an additional day to ensure 7 d of activity monitoring. Another limitation is that the step activity monitor does not quantify nonambulatory physical activity, and therefore it underestimates the total amount of daily physical activity accomplished to some extent. However, we believe nonambulatory activity had minimal effect on the study results because ambulation is a large component of daily activity, and very few subjects indicated during the medical history that they were actively engaged in any type of nonambulatory or resistance training exercise. There is a limitation associated with the assessment of body fat percentage, as bioelectrical impedance analysis technique underestimates fat mass and body fat percentage compared with dual-energy x-ray absorptiometry (28,34), although the measures from both techniques are highly correlated (31). A final limitation is that the present findings only apply to apparently healthy subjects with a wide range in body composition.
Summary, conclusion, clinical significance
In summary, 18% of the subjects in the current study have metabolic syndrome as defined by the International Diabetes Federation, which far exceeds a previously reported prevalence of 3% to 4% in children and adolescents (6) and 6.7% prevalence in adults between 20 and 29 yr (12). Children, adolescents, and young adults with metabolic syndrome have slower cadences during continuous ambulation ranging from 1 min to 1 h, discontinuous ambulation for 30 min, and total ambulation averaged for the entire day than those without metabolic syndrome. Furthermore, body fat percentage and fat mass were the primary factors associated with daily ambulatory activity, particularly with the cadence of ambulation.
In conclusion, children, adolescents, and young adults with metabolic syndrome ambulate more slowly and take fewer strides throughout the day than those without metabolic syndrome, although the total amount of time spent ambulating is not different. Furthermore, the detrimental influence of metabolic syndrome on ambulatory cadence is primarily a function of body fatness. The clinical significance is that children, adolescents, and young adults with metabolic syndrome should be encouraged to ambulate at cadences slightly faster than their preferred pace and for at least 30 additional minutes throughout the course of a day as a simple means to potentially reduce body fatness and to improve glucose, triglyceride, and HDL cholesterol profiles.
This research was supported by the National Center on Minority Health and Health Disparities (grant no. P20-MD-000528-05) and by the University of Oklahoma Health Sciences Center General Clinical Research Center (grant no. M01-RR-14467), sponsored by the National Center for Research Resources from the National Institutes of Health. The final peer-reviewed version of this manuscript is subject to the National Institutes of Health Public Access Policy and will be submitted to PubMed Central.
The authors declare no conflict of interest in the study.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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