Prevalence of Metabolic Syndrome and Individual Criterion in US Adolescents: 2001–2010 National Health and Nutrition Examination Survey

Abstract

Background:

The prevalence of metabolic syndrome has increased in adolescents in previous years. The objectives of this study were to examine the prevalence in the past decade and the individual criteria in a nationally representative sample of US adolescents.

Methods:

This study was a descriptive analysis of 3495 US adolescents between the ages of 12 and 19 years using the National Health and Nutrition Examination Survey (NHANES) 2000–2010. Metabolic syndrome was defined as having three of the five following conditions: Waist circumference (WC),≥90^th percentile (sex-specific); elevated resting blood pressure,≥90^th percentile (age, height, sex-specific); elevated triglycerides (TGs); low high-density lipoprotein cholesterol; and/or impaired fasting glucose.

Results:

Approximately 73.2% of the participants had at least one criterion, with the estimated metabolic syndrome prevalence being 10.1%. Prevalence was higher in males than females (13.0% vs. 6.4%, P<0.05). Both Hispanic males and females had significantly greater odds of metabolic syndrome. Abnormal WC and abnormal TG levels were the most common individual criteria; in comparison, abnormal blood pressure was the least common across racial ethnic backgrounds.

Conclusions:

An estimated one in 10 US adolescents has metabolic syndrome. These findings have important public health implications due to the known cardiovascular disease risk factors associated with metabolic syndrome.

Introduction

Metabolic syndrome is a grouping of cardiovascular disease (CVD) risk factors found in an estimated 36% of the US adult population.¹ These metabolic abnormalities include: (1) Central or general obesity [increased waist circumference (WC)]; (2) hypertension (HTN; elevated or high blood pressure); (3) glucose intolerance, insulin resistance (diabetes), or some level of poor glucose control; (4) a reduced level of high-density lipoprotein-cholesterol (HDL-C); and (5) elevated levels of triglycerides (TGs; hypertriglyceridemia). A combination of at least three or more of these specific metabolic abnormalities in an individual constitutes a diagnosis of metabolic syndrome. Johnson et al.² reported 8.6% of the adolescent population was diagnosed with metabolic syndrome using the National Health and Nutrition Examination Survey (NHANES) data collected between 2001–2006. de Ferranti et al. reported that approximately 1 in 10 children ages 12–19 were diagnosed with metabolic syndrome; however, in overweight adolescents, one in three had metabolic syndrome.³ de Ferranti et al. stated that their results are not surprising considering the increasing rates of obesity and type 2 diabetes mellitus (T2DM) in US children.³

Many overweight children also have elevated glucose levels, suggesting an increase in insulin resistance, which can lead to T2DM.⁴ In addition to being overweight, many studies have reported that adolescents possess at least one or more metabolic abnormality such as hypertriglyceridemia, low HDL-C, or HTN.^4,5 Numerous studies have reported rates of metabolic syndrome in different ethnic populations of children and adolescents in the United States.^6,7 Cruz et al. reported 30% of Hispanic youth were found to be overweight and have greater than or equal to three components of metabolic syndrome.⁷ In a sample of non-Hispanic white, non-Hispanic black, and Hispanic obese adolescents, Weiss et al.⁶ found 39% of the moderately obese adolescents and 50% of severely obese adolescents had three components of metabolic syndrome. Finally, Goodman et al.⁸ reported the prevalence of metabolic syndrome in adolescents using the adult National Cholesterol and Education Program (NCEP) criteria and found that 4.2% met the criteria. The primary aim of this study was to investigate the prevalence of metabolic syndrome in adolescents ages 12–19 years in the United States between 2001 and 2010. A secondary aim was to examine the prevalence of the individual criterion of metabolic syndrome between different sexes and racial ethnic backgrounds.

Methods

Study sample

This cross-sectional study used 10 years of data from the 2001–2010 NHANES, a continuous survey conducted by the National Center for Health Statistics.⁹ The NHANES is representative of the civilian, noninstitutionalized population and is conducted by the Centers for Disease Control and Prevention (CDC). The NHANES is collected in 2-year cycles to provide national estimates of the health and nutrition status of the US population. Informed consent and assent were obtained from all participants prior to testing. The Institutional Review Board at A.T. Still University approved the use of the NHANES data for this research.

The study sample included adolescents ages 12–19 years who reported their ethnicity as Mexican American, Hispanic, non-Hispanic white, non-Hispanic black, and other. The final sample was 3495 US adolescents who met the inclusion criteria: (1) Attended the Mobile Examination Center (MEC) following an overnight fast (minimum of 8 hr); (2) if female, not pregnant; (3) had complete data of all study variables (i.e., glucose, lipoproteins, blood pressure, and WC; and (4) no previous diagnosis of diabetes. All data were collected by trained staff and included the in-home interview questionnaires and standardized medical examinations.

Data for diagnosing metabolic syndrome

Physiological biomarkers included measurement of WC measured to the nearest 0.1 cm at the end of a normal expiration with a steel tape measure placed at the highest point of the iliac crests while in a standing position. Blood pressure was measured after 5 min of rest in the sitting position using the right arm. Measurements were taken up to four times with a mercury sphygmomanometer; the mean of the measurements taken was used in the analysis. Glucose concentration was determined by a hexokinase method, TGs concentration was measured enzymatically using a series of coupled reactions, and HDL-C concentration was measured directly.¹⁰ Adolescents were classified as having metabolic syndrome if they had three or more of the following criteria: (1) WC,≥90^th percentile for their age and sex according to 1988–1994 NHANES III data¹¹; (2) either systolic (SBP) or diastolic (DBP)≥90^th percentile for their height, age, and sex¹²; (3) TGs concentration>110 mg d/L; (4) HDL-C concentration<40 mg d/L; and (5) fasting glucose concentration>100 mg d/L. The criteria used to define metabolic syndrome are the same as those used by Ford et al.¹³

Diagnostic criteria for metabolic syndrome

A metabolic syndrome risk score (MSRS) was calculated for each study participant.¹ The MSRS ranged from a score of 0 to 5. Those participants who scored two or less risk factors were determined not to have metabolic syndrome; in contrast, participants who had three to five risk factors were determined to have metabolic syndrome.

Statistical analysis

Forty-two data files were downloaded from the NHANES web page.¹⁴ These data were managed using SPSS version 21 (IBM, Armonk, NY). SPSS was used to conduct the complex variable recodes and analyze the data.

Data were analyzed as weighted and unweighted. The unweighted analyses assumed the sample cases were based upon the participants who were recruited over the 10 years. Weighted analyses assumed the sample cases were based on the entire population of adolescents in the United States. SPSS was used to determine the prevalence of metabolic syndrome and at risk values (high and low measurements) in the five-component variable used to classify adolescents with metabolic syndrome. Estimates of the number of adolescents in various subpopulations were also reported. Prevalence data expressed as a percentage with 95% confidence intervals (CIs), weighted to be nationally representative, were compiled for the overall sample, males and females, racial/ethnic groups, and within sex-ethnic groups. Ethnicity was categorized as Hispanic (Mexican American, Hispanic, and other Hispanics), non-Hispanic white, non-Hispanic black, and other. Overall and sex-specific trends were evaluated during the data collection periods 2001–2002 to 2009–2010.

Results

The sample demographic characteristics of the study population of eligible (n=3495) US adolescents from the NHANES database represented approximately 33.9 million adolescents when weighted (Table 1). The sample population was weighted to reflect the base probabilities of selection, adjustment for nonresponse, and poststratification. Males comprised more than 50% of the weighted sample. The population breakdown was 62.1% non-Hispanic white, 16.7% Hispanic, 14.7% non-Hispanic black, and 6.6% other ethnicities.

Table 1.

Sample Demographics Characteristics (Unweighted and Weighted), NHANES 2001–2010 (n=3495)

Characteristic	Study sample n (95% CI)	Population estimate (×1000)	%
Total	3495	33,950
Gender
Male	1624 (44.3,48.3)	17,207	50.7
Female	1871 (51.9, 55.2)	16,742	49.3
Age at screening, (years)
12–13	881 (23.8, 26.7)	7,824	23.0
14–15	869 (23.5, 26.3)	8,908	26.3
16–17	893 (24.1, 27.0)	8,775	25.8
18–19	852 (23.0, 25.8)	8,440	24.9
Race/ethnicity
Non-Hispanic white	1010 (27.4, 30.4)	21,082	62.1
Non-Hispanic black	1043 (28.4, 31.4)	4,977	14.7
Hispanic	1272 (34.8, 38.0)	5,660	16.7
Other	170 (4.1, 5.6)	2,229	6.6

NHANES, National Health and Nutrition Examination Survey; CI, confidence interval.

Prevalence of metabolic syndrome sex and ethnicity

The overall prevalence of metabolic syndrome in adolescents was 10.1% of the population sample (Table 2), which represents 3.3 million adolescents in the general population. It was more common in males (12.9%) than in females (6.9%) (P<0.001) and more prevalent in Hispanic male (18.0%) (P<0.001), non-Hispanic white male (15.5%) (P<0.001), other ethnicity male (10.1%) (P=0.203), Hispanic female (10.1%) (P=0.06), non-Hispanic white female (6.8%), non-Hispanic black male (6.5%) (P=0.235), other ethnicity female (4.0%) (P=0.455), non-Hispanic black female (3.2%) (P=0.016) adolescents when compared to a non-Hispanic white female.

Table 2.

Population Prevalence of Metabolic Syndrome in US Adolescents Aged 12–19 years (Unweighted)

Characteristic	n (%)	Overall %	95% CI	Male n (%)	Male 95% CI	Overall male %	Female n (%)	Female 95% CI	Overall female %
Metabolic syndrome, three or more of five criteria		10.1				12.9			6.9
Hispanic	181 (14.6)	26.8	12.4, 16.3	119 (18.0)	15.2, 21.1	18.0	62 (10.1)	8.0, 12.8	10.1
Non-Hispanic white	116 (9.8)	62.7	9.7, 13.6	84 (15.5)	6.8, 10.2	15.5	32 (6.8)	4.9, 9.5	6.8
Non-Hispanic black	44 (5.2)	7.1	3.2, 5.6	29 (5.1)	3.5, 7.2	6.5	15 (3.2)	2.0, 5.2	3.2
Other	13 (7.6)	3.5	4.5, 12.7	10 (10.5)	5.8, 18.3	10.1	3 (4.0)	1.4, 11.1	4.0
WC,≥90^th percentile		40.8				37.5			44.5
Hispanic	597 (46.9)	41.9	44.2, 49.7	300 (45.4)	41.6, 49.1	42.7	297 (48.6)	44.7, 52.6	41.1
Non-Hispanic white	417 (41.3)	29.3	38.3, 44.4	218 (40.3)	36.3, 44.5	31.1	199 (42.4)	38.0, 47.0	27.5
Non-Hispanic black	358 (34.3)	25.1	31.5, 37.3	152 (26.5)	23.0, 30.2	21.7	206 (43.9)	39.5, 43.9	28.5
Other	53 (31.2)	3.7	2.5, 38.5	32 (33.7)	25.0, 43.7	4.6	21 (28.0)	19.1, 39.0	2.9
Blood pressure,≥90^th percentile		4.9					5.3		4.5
Hispanic	41 (3.2)	23.7	2.4, 4.3	24 (3.6)	2.5, 5.3	24.0	17 (2.8)	1.7, 4.4	23.3
Non-Hispanic white	45 (4.5)	26.0	3.4, 5.9	25 (4.6)	3.2, 6.7	25.0	20 (4.3)	2.3, 6.5	27.4
Non-Hispanic black	83 (8.0)	48.0	6.5, 9.8	48 (8.4)	6.4, 10.9	48.0	35 (7.5)	5.4, 10.2	47.9
Other	4 (2.4)	2.3	0.9, 5.9	3 (3.2)	1.1, 9.9	3.0	1 (1.3)	0.2, 7.2	1.4
Triglycerides,≥110 mg/dL		20.6				22.3			18.6
Hispanic	324 (25.5)	45.0	23.2, 27.9	182 (27.5)	24.2, 31.1	43.5	142 (23.2)	20.1, 26.8	47.0
Non-Hispanic white	274 (27.1)	38.1	24.5, 30.0	161 (29.8)	26.1, 33.7	38.5	113 (24.1)	20.4, 28.2	37.4
Non-Hispanic black	93 (8.9)	12.9	7.3, 10.8	55 (9.6)	7.4, 12.3	13.2	38 (8.1)	6.0, 10.9	12.6
Other	29 (17.1)	4.0	12.3, 23.4	20 (21.1)	14.1, 30.3	4.8	9 (12.0)	6.4, 21.3	3.0
HDL-C,≤40 mg/dL		16.1				19.9			11.8
Hispanic	234 (18.4)	41.6	16.7, 20.6	154 (23.3)	20.2, 26.6	41.4	80 (13.1)	10.6, 16.0	41.9
Non-Hispanic white	201 (19.9)	35.7	17.6, 22.5	140 (25.9)	22.4, 29.7	37.6	61 (13.0)	10.3, 16.4	31.9
Non-Hispanic black	107 (10.3)	19.0	8.6, 12.3	63 (11.0)	8.7, 13.8	16.9	44 (9.4)	7.1, 12.4	23.0
Other	21 (12.4)	3.7	8.2, 18.1	15 (15.8)	9.8, 24.4	4.0	6 (8.0)	3.7, 16.4	3.1
FG,≥100 mg/dL		16.5				22.2			9.9
Hispanic	269 (21.1)	46.6	19.0, 23.5	192 (29.0)	25.7, 32.6	46.2	77 (12.6)	10.2, 15.5	47.8
Non-Hispanic white	167 (16.5)	28.9	14.4, 19.0	121 (22.4)	19.1, 26.1	29.1	46 (9.8)	7.4, 12.8	28.6
Non-Hispanic black	110 (10.5)	19.1	8.8, 12.6	80 (13.9)	11.4, 17.0	19.2	30 (6.4)	4.5, 9.0	18.6
Other	31 (8.2)	18.2	13.2, 24.7	23 (24.2)	16.7, 33.7	5.5	8 (10.7)	5.5, 19.7	5.0

CI, confidence interval; WC, waist circumference; BP, blood pressure; HDL-C, high-density lipoprotein cholesterol; FG, fasting glucose.

Prevalence of individual risk factors by ethnicity

Overall, abnormal WC and abnormal TG levels were the most common individual criteria; in contrast, abnormal blood pressure was the least common criterion across the different race and ethnic groups. Hispanic adolescents had the highest rates of abnormal WC (46.9%) and fasting glucose (21.1%). Non-Hispanic white adolescents had the highest rates of abnormal TGs levels (27.1%) and abnormal HDL-C levels (19.9%). Non-Hispanic black adolescents had the highest rates of abnormal blood pressure (8.0%) (Table 2).

Prevalence of risk factor combinations

Two-thirds (66.7%) of adolescents had at least one metabolic abnormality, and 10.1% met the criteria for diagnosis of metabolic syndrome (Table 3). Four or more individual criteria were found in 103 adolescents (1.1%); 12 adolescents had all five criteria (0.1%). More females had at least one metabolic abnormality when compared with males (50.9% vs. 49.1%). However, 13.0% of males compared with 7.0% of females had three or more criteria components for metabolic syndrome (Table 3).

Table 3.

Prevalence of Individual Criterion in Adolescent Males and Females with Metabolic Syndrome

	0	1	2	3	4	5
Male	39.9%	30.4%	16.7%	8.8%	3.7%	0.5%
Female	41.4%	36.3%	15.4%	5.5%	1.4%	0.1%

Metabolic Risk Stratification Score (MRSS): 0=no individual criteria met; 5=all individual criterion met.

Discussion

Metabolic syndrome is prevalent in today's society. This syndrome affects adults, but current views indicate that metabolic syndrome starts in childhood and adolescence. When examining earlier research, the findings of this study demonstrate that the prevalence of metabolic syndrome has increased over the past decade.^2,3,15 There is still variability between the criteria used to define metabolic syndrome in adolescents. Using the latest available NHANES data (2001–2010), our estimated overall prevalence of metabolic syndrome in adolescents was 10.1%. Overall, Hispanic adolescents (14.6%) had the greatest prevalence, followed by non-Hispanic white (9.8%), other ethnicity (7.6%), and non-Hispanic black (5.2%) adolescents. The overall prevalence was significantly higher in males than females. Abnormal WC and TGs were the most prevalent between the sexes and ethnicities, whereas HTN was lowest.

The results of this study build on previous studies that have shown the prevalence of metabolic syndrome in adolescents has increased.^2,3,15 The prevalence of metabolic syndrome in this study was 10.1% of US adolescents compared to Johnson et al.² (10.1% vs. 8.6%), Cook et al.¹⁵ (10.1% vs. 4.1%), and de Ferranti et al.³ (10.1% vs. 9.2%). During the years 1988–1994, the estimated prevalence of metabolic syndrome was 4.2% in US adolescents.¹⁵ Nearly 5 years later, the prevalence of metabolic syndrome increased and was estimated to be 6.4% during 1999–2000.¹⁶ Ford et al. estimated that 3.8% of adolescents had metabolic syndrome in 1999–2000.¹⁷ Other researchers have reported prevalence of metabolic syndrome in adolescents between 2.0% and 8.6% of the population.^2,6,7 Johnson et al. reported that metabolic syndrome occurred in nearly 2.5 million adolescents when extrapolated to the general population during 2001–2006.² The increase in the prevalence of metabolic syndrome further emphasizes that monitoring metabolic syndrome in adolescents is warranted to help reduce the risk of future CVD and T2DM in adulthood.

Among non-Hispanic black males the prevalence of abnormal WC was 26.5%, but it exceeded 28.0% in all other sex and ethnic groups in the present study. Prevalence of abnormal TGs was highest in non-Hispanics and Hispanics in both sexes, and lowest in non-Hispanic blacks. Abnormal fasting glucose was highest in Hispanic, non-Hispanic white, and other ethnicity males compared to females of the same ethnicities. The prevalence of low HDL-C was highest in non-Hispanic and Hispanic males, respectively, with approximately half as many females having this condition. Elevated resting blood pressure had the lowest prevalence in all ethnicities and sexes. Johnson et al. reported similar findings of blood pressure being the lowest metabolic abnormality in adolescents independent of their ethnicity or sex.²

The clustering of metabolic abnormalities leads to the definition of metabolic syndrome. However, the prevalence of these individual factors during adolescence in the United States has been increasing over recent years.^2,18 Johnson et al. estimated that nearly 42% of adolescents had one or two metabolic abnormalities.² It was also determined that nearly 8.6% of this population had at least three risk factors. In the present study we found that nearly 47% of adolescent males had at least one or two metabolic abnormalities, whereas 51% of adolescent females had at least one or two metabolic abnormalities. More males than females possessed at least one metabolic abnormality (55.5% vs. 45.5%). Freedman et al. examined various cutoff points in identifying children with excess adiposity (based upon skinfold thickness), adverse levels of lipids, insulin, and blood pressure, and a high risk for severe adult obesity.⁴

In the Bogalusa Heart Study, which tested participants as children and followed them for 10 years, it was determined that 26% of the children had at least one metabolic syndrome risk factor and 4% had three or more risk factors.¹⁹ A comparison between the two studies demonstrates nearly a doubling in the prevalence of one risk factor as well as three or more risk factors.^4,18 A major conclusion that Kranz et al. state was that those children who had higher body mass index (BMI) values relative to their sex and age peers are more likely to have multiple risk factors, excess adiposity, and a high risk for adult obesity.¹⁸ Freedman et al. also demonstrated that those children with higher BMI values were more likely to be classified as obese or morbidly obese as adults.⁴ These findings indicate that children and adolescents that are at risk for being overweight or currently overweight have a greater likelihood of developing metabolic syndrome as adults.

Bao et al. used data from the Bogalusa Heart Study and retested the participants 8 years later to determine if the clustering of risk factors in childhood continued into adulthood.¹⁹ This study demonstrated the prevalence of cardiovascular risk factors cluster in children and young adults, but the clustering persists into adulthood. Bao et al. found those children who were classified as obese had clustering of the components for metabolic syndrome compared to leaner children.¹⁹ The prevalence of multiple risk factors for metabolic syndrome will follow a child into adolescence and into adulthood if there are no lifestyle changes. Clustering of metabolic abnormalities, regardless of the age of an individual, increases the risk of metabolic syndrome.

The potential for early onset of puberty in adolescents may potentially increase the risk for metabolic syndrome.²⁰ This impact can be found with a delay of pubertal onset and taller stature in males, whereas females are more likely to have earlier thelarche (breast development).²¹ Changes in the hormone regulation of appetite, satiety, and fat distribution occurring during puberty may put adolescents at increased risk for additional weight gain. Two hormones that play a large role in the timing of puberty and its progression are leptin and insulin. Overweight and obese adolescents will have higher levels of leptin, and higher levels of insulin may cause insulin resistance that can lead to T2DM.

There are limitations in the present study that need to be addressed. The primary limitation was the cross-sectional nature of the data; only associations, not causality, could be examined. The cross-sectional nature of the NHANES survey does not allow us to make causal inferences as to the underlying relationship between developing an increased WC and metabolic syndrome in adolescents. However, because both conditions have continued to increase, our findings point to major changes in lifestyle, such as poor diet and physical inactivity, as major contributors to the increased prevalence of metabolic syndrome in adolescents. Second, presently there is not a consensus definition for metabolic syndrome in adolescents. There are numerous definitions that have been adapted from adult definitions for children and adolescents.^{2,3,15,17,22
–24} These working definitions have modified adult definitions of metabolic syndrome to an adolescent population. Last, oversampling of population subgroups was changed and adolescents are no longer oversampled since 2004. The reduction in oversampling may reduce the observed differences among gender-ethnic subgroups and may be smaller due to the reduced numbers of populations surveyed because their numbers are much larger than believed.

The study findings suggest the prevalence of metabolic syndrome has increased over the past decade. Abnormal WC and TGs continually are the most prevalent issues among adolescents today. Presently, it is estimated that one in 10 US adolescents has metabolic syndrome. These findings have important public health implications due to the well-known CVD risk factors associated with metabolic syndrome that may be carried into adulthood. To reduce the potential future risk of CVD in these future adults, adolescents with a current diagnosis of metabolic syndrome should reduce energy intake, increase physical activity, and limit sedentary behaviors.

Footnotes

Author Disclosure Statement

No competing financial interests exist. The authors have no disclosures to make in relation to the content of this manuscript.

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