The alarming increase in obesity among the youth and adolescents warrants an updated review of the metabolic syndrome (MetS) in youth, particularly minority adolescents. The effect of obesity on the risk for cardiovascular disease (CVD) is mediated to a large extent by its effects on MetS and its component risk factors. Previous studies have resulted in different findings, in part because of the difficulty of coming to an agreement on the most appropriate criteria to use and also because data are limited with regard to recent trends, particularly among youth and adolescents 1.
Over the last 30 years, a growing change in food consumption habits from undernutrition to overnutrition and a decrease in physical activity have been seen primarily in the industrial and technologically advanced countries 2,3. In the USA, the increasing prevalence of overweight adolescents, particularly among the ethnic minority groups such as African–Americans and Hispanics, has been well established 4,5. Further, the ethnic minority population in the USA has a higher frequency of diabetes and its respective risk factors compared with Caucasians. Before 1994, type 2 diabetes was uncommon among children and adolescents, but recently the prevalence has increased in conjunction with increasing overweight and obesity levels. With respect to CVD, the increase in obesity rates among the youth has tripled since 1980 5. As obesity has been associated with all the risk factors of MetS and the rising prevalence of overweight and obesity in children and adolescents has increased since 1999–2000 National Health and Nutrition Examination Surveys (NHANES; from 14.3% in 1999–2000 to 16.6% in 2005–2006) 6, there is an urgent need to report the prevalence of MetS using modern criteria, particularly among minority adolescents.
This study addresses the prevalence of MetS and its associated risk factors on the basis of data gathered from the 1999–2008 NHANES, with a primary focus on minority participants and the roles that sex, age, and ethnicity may play in the prevalence of MetS and its associated risk factors. In addition, comparison of the prevalence recorded in earlier NHANES allows for examining the trends in the prevalence of MetS in recent years.
We studied 11 024 individuals, aged between 10 and 18 years, of Hispanic, non-Hispanic white, non-Hispanic black, or unidentified ethnicities in the NHANES from 1999 to 2008. These individuals represent over 186 million people in the USA with regard to sample weight. All individuals had sufficient risk factors to determine the presence or absence of MetS on the basis of the modified National Cholesterol Education Program Adult Treatment Panel III definition, according to which elevated levels of triglycerides, systolic or diastolic blood pressure, and glucose or an increased waist circumference was based on being at or above the 85th percentile [and below the 15th percentile for high-density lipoprotein (HDL) cholesterol], as has been suggested previously to modify the adult standards to those suitable for the youth 7,8.
Lipids were analyzed in serum and plasma using coupled reactions that hydrolyzed esters and oxidized the 3-OH group of cholesterol. Serum triglyceride and HDL cholesterol levels were measured enzymatically and after using a chloride mixture to precipitate other lipoproteins on a Hitachi 704 analyzer (Boehringer Mannheim Diagnostics, Indianapolis, Indiana, USA). The concentration of plasma glucose was measured by an enzymatic reaction (Cobas Mira Chemistry System; Roche Diagnostic Systems, Montclair, New Jersey, USA). Blood pressure was measured using a mercury sphygmomanometer and the average of four readings was calculated.
The standard defining MetS for the 1999–2000 NH4 dataset was the modified National Cholesterol Education Program Adult Treatment Panel III definition 7, represented at the 85th percentile cutoff points (or below the 15th percentile for HDL cholesterol). Under these criteria, MetS was defined on the basis of the presence of at least three of the of the following risk factors: waist circumference greater than 95.6 cm for boys and greater than 92.5 cm for girls; triglyceride levels of 127 mg/dl or more for boys and 121 mg/dl or more for girls after at least 8 h of fasting; HDL cholesterol levels less than 37 mg/dl for boys and less than 40 mg/dl for girls; blood pressure of at least 122/73 mmHg for boys and at least 16/73 mmHg for girls; and/or a glucose level of 95 mg/dl or more for boys and 90 mg/dl or more for girls after at least 8 h of fasting. The same criteria were used in determining the prevalence of MetS in the 2001–2008 NHANES datasets.
Cross-tabulation procedures applied in SUDAAN software were used to determine the population-weighted prevalence of MetS. The χ2-test of proportions and analysis of variance were used for comparing differences in the prevalence of MetS and its associated risk factors with regard to sex, age, and ethnicity. The Cochran–Mantel–Haenszel test was used to examine the trend of MetS prevalence from 1999 to 2008. SAS statistical software version 9.1.3 (SAS Institute, Cary, North Carolina, USA) was used to carry out all analysis, with SUDAAN version 10.0.1 (Research Triangle Institute, Research Triangle Park, North Carolina, USA) used for sample weighting for projection of our study sample to the US population.
Among our adolescent population, the overall prevalence of MetS was 3.5% in 1999–2000, without significant increases in 2007–2008 (3.8%; Table 1). In the five survey periods, there were no significant changes overall or between sexes in terms of MetS prevalence (Fig. 1). Individuals between 10 and 13 years and those between 14 and18 years old showed significant differences in all surveys, with the prevalence being 5% or more in those aged between 15 and 18 years. In terms of ethnicity, significant differences were observed during three periods, 2001–2002, 2005–2006, and 2007–2008, with the latter two periods showing the highest prevalence in Hispanics. A significant, increasing trend is shown only by Hispanic youth from 1999 to 2008, with an increase in prevalence from 3.5 to 7.6% (trend P<0.001; Table 1 and Fig. 2).
Comparison of MetS risk factor prevalence by sex, age group, and ethnicity (Table 2) showed that most risk factors were of similar frequency among boys and girls, except that boys were more likely to have elevated triglyceride levels and less likely to have impaired fasting glucose levels compare with girls. Moreover, among younger (aged 10–13 years) versus older (aged 14–18 years) children, increased waist circumference, low HDL cholesterol levels, elevated triglyceride levels, elevated blood pressure levels, and impaired fasting glucose levels were significantly less common in most, if not all five, surveys. Among ethnic groups, there were significant differences in the prevalence of elevated triglyceride levels across ethnic groups (being more than twice as common in both non-Hispanic white and Hispanic children compared with non-Hispanic blacks); low HDL cholesterol levels (being most common in non-Hispanic blacks) and high abdominal obesity were most common among Hispanics. Among non-Hispanic blacks, high abdominal obesity was the most common metabolic risk factor (16.3 and 14.7%, P<0.001), whereas among non-Hispanic whites it was elevated triglyceride levels (15.3%, P<0.001). Impaired fasting blood glucose and elevated triglyceride levels show some significant, increasing trends for different sexes, age groups, and ethnicities over a 10-year period, whereas the opposite is seen for the prevalence of low HDL cholesterol levels. Of note, among Hispanics, the prevalence of impaired fasting glucose levels increased from 15.4% in 1999–2000 to 22.5% in 2007–2008 (P<0.001) and that of elevated triglyceride levels increased from 14.3 to 17.9% (P<0.001).
Mean levels of metabolic syndrome risk factors were also compared by sex, age group, and ethnicity (Table 3). Boys had lower levels of HDL cholesterol, but higher levels of systolic and diastolic blood pressure, triglycerides, and fasting blood glucose compared with girls. In younger compared with older children, although waist circumference and systolic and diastolic blood pressures were lower, HDL cholesterol and fasting blood sugar levels were higher. Across ethnic groups, Hispanics had the largest waist circumference, whereas African–American children had the highest levels of HDL cholesterol and systolic blood pressure and the lowest level of triglycerides. A decreasing trend for diastolic blood pressure and an increasing trend for fasting blood glucose are shown for Hispanic youth between 1999 and 2008.
Our data show that among youth and adolescents in the USA during 1999–2008, Hispanics show significant increases in the prevalence of MetS; however, there were no demonstrable increases overall among different sexes or age groups. Increased abdominal obesity and triglyceride levels and impaired fasting glucose levels were the most common risk factors for MetS, with associated increases in impaired fasting glucose levels, particularly among Hispanics, during the survey periods.
Clearly, obesity is a core risk factor for chronic conditions in both adults and youth. It is associated with the development of hypertension, diabetes mellitus, and hyperlipidemia and results in insulin resistance, with subsequent hyperinsulinemia, in part through the role of intra-abdominal fat, which can be estimated from waist circumference and may be related to the insulin resistance syndrome 9–11. As estimation of BMI is the most frequently used method for obesity measurement in health and medical settings, it should be noted that it is age and sex specific and does estimate adolescent body fat. Results support the determination of the prevalence of MetS by estimation of adiposity, as the results are concordant with previous findings.
Maffies et al.12 suggested that waist circumference may be a valuable tool for estimation of health risk associated with obesity in children, and the findings support this contention. Studies by Caprio and colleagues 13,14 have suggested that, in adolescents, accumulated visceral fat is more closely related to glycemic status than overall obesity; however, others do not agree 15. Although there is no significant change in waist circumference in this dataset, there is a significant change in fasting blood glucose levels. Waist circumference is reproducible when measurements are made by trained personnel, and it relates more to visceral body fat, which has been shown to be more clinically relevant in diagnosing adults 16,17. Ball et al.18 provide findings supporting waist circumference as the greatest correlate to visceral adipose tissue. As visceral fat is difficult to measure directly, waist circumference should be measured by trained personnel in order to obtain accurate values. Waist circumference has been used as a surrogate for abdominal adiposity. However, the most accessible and convenient and least sensitive measure used clinically to estimate overweight and obesity in adolescents is the age-specific and sex-specific BMI 19. Despite this, the relationship between BMI and obesity is different between boys and girls, particularly among older adolescents 20. Taylor et al.21 have shown that BMI can considerably overpredict body fat percentage of adolescents, particularly in girls. Thus, BMI may be a less-than-perfect measure for assessing body fat content and prevalence of MetS.
Lipid levels have been shown to vary by ethnicity among children, with higher total cholesterol and low-density lipoprotein cholesterol being reported among non-Hispanic blacks compared with non-Hispanic whites and Hispanics 22. Higher blood pressure levels have also been reported among non-Hispanic black children compared with non-Hispanic white and Hispanic children. Total cholesterol, triglyceride, HDL cholesterol 15, and blood pressure levels have been shown to vary according to the developmental stage (as defined by age group). The sex gap clearly demonstrates that adolescent girls have the least favorable profile. Yet, risk factor treatment should not be sex exclusive as sex differences in both lipid and blood pressure values have been reported with higher total cholesterol levels among girls and higher systolic blood pressure levels among boys 23. In terms of race, national health survey data over the last two decades have shown that the highest prevalence 24 and steepest secular rise 25 in hypertension is among black youth (especially boys). Age group analysis shows that prevalence increases as adolescents grow older, which is consistent with previous findings 7,26. Prevalence among Hispanics is high, as reported in previous studies 27, whereas other minorities continue to have lower values. In this dataset, although there is no significant change in waist circumference, there is a significant change in diastolic blood pressure. Overall, MetS is suggested to be a diagnostic tool in predicting cardiometabolic risk in children rather than being an individual disease 28. Our results showed a significant change in the prevalence of MetS among Hispanics between 1999 and 2008. Hispanic youth appear to be the only group with an increasing prevalence of MetS. This trend solicits attention as Hispanic youth with increased MetS risk factors have been found to be at a higher risk for CVD and insulin resistance 29. Clustering of metabolic risk factors during childhood predicts the development of MetS into adulthood, indicating the significance of longer-term health implications.
Our study has several strengths and limitations. An important strength is that the study sample is representative of all children and adolescents in the US population, representing whites, blacks, and Hispanics; however, unfortunately, NHANES does not categorize other important ethnic groups in the US, such as Asians. In addition, NHANES has standardized risk factor measures that ensure comparability across survey sites in the USA as well as between study periods. One limitation is our inability to follow-up participants on the occurrence of diabetes, as NHANES is a cross-sectional rather than a longitudinal survey.
Our study notes that although the overall prevalence of MeS in children and adolescents has not markedly increased over the past decade, there is a significant increase in the prevalence of MetS among Hispanics, which may be closely related to the increase in the prevalence of impaired fasting glucose and elevated triglycerides levels in particular. This will continue to fuel the impending epidemic of type 2 diabetes among the youth and adolescents, and our data suggest that this will be of greatest concern among Hispanics. Our findings support the immediate implementation of public policy changes according to which fiscal and human resources should be committed to developing school and community integrated strategies to blunt the unhealthy profile nationwide. The challenge for future public health research and intervention efforts like Project Healthy 30 may be in devising strategies that target high-risk youth who are ethnically and culturally specific and sensitive.
Conflicts of interest
Dr Wong has received research support from Merck and Bristol Myers-Squibb through the University of California, Irvine.
1. Weiss R, Dziura J, Burgert TS, Tamboralane WV, Taksali SE, Yeckel CW, et al. Obesity and the metabolic syndrome
in children and adolescents. N Engl J Med. 2004;350:2362–2374
2. Heimburger DC, Allison DB, Goran MI, Heini AF, Hensrud DD, Hunter GR, et al. A festschrift for Roland L Weinsier: nutrition scientist, educator, and clinician. Obes Res. 2003;11:1246–1262
3. Keith SW, Redden DT, Katzmarzyk PT, Boggiano MM, Hanlon EC, Benca RM, et al. Putative contributors to the secular increase in obesity: exploring the roads less traveled. Int J Obes. 2006;30:1585–1594
4. Ogden CL, Flegal KM, Carroll MD, Johnson CL. Prevalence and trends in overweight among US children and adolescents, 1999–2000. JAMA. 2002;288:1728–1732
5. Ogden CL, Carroll MD, Curtin LR, Lamb MM, Flegal KM. Prevalence of high body mass index in US children and adolescents, 2007–2008. JAMA. 2010;303:242–249
6. Hedley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR, Flegal KM. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999–2002. JAMA. 2004;291:2847–2850
7. Jolliffe CJ, Janssen I. Development of age-specific adolescent metabolic syndrome
criteria that are linked to the Adult Treatment Panel III and International Diabetes Federation criteria. J Am Coll Cardiol. 2007;49:891–898
8. . Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA. 2001;285:2486–2487
9. Eckel RH, Krauss RM. American Heart Association call to action: obesity as a major risk factor for coronary heart disease. Circulation. 1998;97:2099–2100
10. Sjostrom LV. Mortality of severely obese subjects. Am J Clin Nutr. 1992;55:516S–523S
11. Krauss RM, Winston M, Fletcher BJ, Grundy SM. Obesity: impact on cardiovascular disease
. AHA conference proceedings. Circulation. 1998;98:1472–1476
12. Maffeis C, Grezzani A, Pietrobelli A, Provera S, Tato L. Does waist circumference predict fat gain in children? Int J Obes. 2001;25:978–983
13. Caprio S, Hyman LD, Limb C, McCarthy S, Lange R, Sherwin G, Tamborlane WV. Central adiposity and its metabolic correlates in obese adolescent females. Am J Physiol. 1995;269:E118–E126
14. Caprio S, Bronson M, Sherwin RS, Rife F, Tamborlane WV. Coexistance of severe insulin resistance and hyperinsulinaemia in pre-adolescent obese children. Diabetologia. 1996;39:1489–1497
15. Roemmich JN, Clark PA, Luck M, Friel A, Weltman A, Epstein LH, Rogol AD. Pubertal alterations in growth and body composition. IV. Pubertal insulin resistance: relation to adiposity, body fat distribution and hormone release. Int J Obes. 2002;26:701–709
16. Maffeis C, Moghetti P, Grezzani A, Clementi M, Guadino R, Tato L. Insulin resistance and the persistence of obesity from childhood into adulthood. J Clin Endocrinol Metab. 2002;87:71–76
17. Taylor RW, Jones IE, Williams SM, Goulding A. Evaluation of waist circumference, waist-to-hip ratio, and the conicity index as a screening tool for high trunk fat mass, as measured by dual-energy X-ray absorptiometry, in children aged 3–19 year. Am J Clin Nutr. 2000;72:490–495
18. Ball GD, Huang TT, Cruz ML, Shaibi GQ, Weigensberg JM, Goran MI. Predicting abdominal adipose tissue in overweight Latino youth
. Int J Ped Obes. 2006;1:210–216
19. Kiess W, Galler A, Reich A, Müller G, Kapellen T, Deutscher J, et al. Clinical aspects of obesity in childhood adolescence. Obes Rev. 2001;2:29–36
20. Lindsay RS, Hanson RL, Bennett PH, Knowler WC. Secular trends in birth weight, BMI, and diabetes in the offspring of diabetic mothers. Diabetes Care. 2000;23:1249–1254
21. Taylor RW, Jones IE, Williams SM, Goulding A. Body fat percentages measured by dual-energy X-ray absorptiometry corresponding to recently recommended body mass index cutoffs for overweight and obese children and adolescents aged 3–18 year. Am J Clin Nutr. 2002;76:1461–1421
22. Freedman DS, Dietz WH, Srinivasan SR, Berenson GS. The relation of overweight to cardiovascular risk factors
among children and adolescents: the Bogalusa Heart Study. Pediatrics. 1999;103:1175–1182
23. Nicklas TA, von Duvillard SP, Berenson GS. Tracking of serum lipids and lipoproteins from childhood to dyslipidemia in adults: The Bogalusa Heart Study. Int J Sports Med. 2002;23(Suppl):s39–s43
24. Din-Dzietham R, Liu Y, Bielo M-V, Shamsa F. High blood pressure trends in children and adolescents in national surveys, 1963 to 2002. Circulation. 2007;116:1488–1496
25. Muntner P, He J, Cutler JA, Wildman RP, Whelton PK. Trends in blood pressure among children and adolescents. JAMA. 2004;291:2107–2113
26. Ford ES, Giles WH, Dietz WH. Prevalence of the metabolic syndrome
among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA. 2002;287:356–359
27. Cook S, Weitzman M, Auinger P, Nguyen M, Dietz W. Prevalence of a metabolic syndrome
phenotype in adolescents: findings from the Third National Health and Nutrition Examination Survey, 1988–1994. Arch Pediatr Adolesc Med. 2003;157:821–827
28. Ferrannini E. Metabolic syndrome
: a solution in search of a problem. J Clin Endocrinol Metab. 2007;92:396–398
29. Cruz ML, Weigensberg MJ, Huang TT, Ball G, Shaibi GQ, Goran MI. The metabolic syndrome
in overweight Hispanic youth
and the role of insulin sensitivity. J Clin Endocrinol Metab. 2004;89:108–113
30. . A school-based intervention for diabetes risk reduction. N Engl J Med. 2010;363:443–453