High Prevalence of the Metabolic Syndrome in Iranian Adolescents

Authors


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Endocrine Research Center, Shaheed Beheshti University of Medical Sciences, PO Box 19395-4763, Tehran, Iran. E-mail: azizi@erc.ac.ir

Abstract

Objective: No evidence exists regarding the prevalence of the metabolic syndrome in adolescents in Middle Eastern countries. We aimed to evaluate the prevalence of the metabolic syndrome in a representative sample of Iranian adolescents.

Research Methods and Procedures: Anthropometry, biochemical measurements, and blood pressure were assessed in a population-based cross-sectional study of 3036 Iranian adolescents (1413 boys and 1623 girls) 10 to 19 years of age. Metabolic syndrome was defined according to modified Adult Treatment Panel III definition. Overweight (≥95th percentile) and at risk for overweight (≥85th to <95th percentile) was defined based on the standardized percentile curves of BMI suggested for Iranian adolescents.

Results: The prevalence of the metabolic syndrome was 10.1% (95% confidence interval: 9.0 to 11.1) among Iranian adolescents (boys: 10.3%, 8.6 to 11.8; girls: 9.9%, 8.4 to 11.3). Overall, low serum high-density lipoprotein-cholesterol and high serum triglycerides were the most common components of the metabolic syndrome (42.8% and 37.5%, respectively). Overweight subjects had the highest proportion of metabolic syndrome compared with those at risk for overweight and those with normal weight (boys: 41.1% vs. 11.4% and 3.0%, respectively, p < 0.01; girls: 43% vs. 15.2% and 5.0%, respectively, p < 0.01).

Discussion: This study provides evidence showing a high prevalence of the metabolic syndrome in Iranian adolescents, particularly among overweight adolescents.

Introduction

Individuals with metabolic syndrome are at increased risk for cardiovascular disease. Metabolic syndrome is defined as a pattern of metabolic disturbances including central obesity, insulin resistance and hyperglycemia, dyslipidemia, and hypertension (1). The third report of the National Cholesterol Education Program Adult Treatment Panel III (ATP III)1 recognized the metabolic syndrome as a secondary target of risk-reduction therapy (2). A recent study in Tehran showed that the metabolic syndrome is highly prevalent in Tehranian adults, with an estimated prevalence of >30% in adults (3), which is higher than that in most developed countries such as the United States (4).

Previous studies indicated that the process of atherosclerosis starts at an early age and is already linked to obesity and other components of the metabolic syndrome in childhood (5). Although the prevalence (3, 4) and associated risk factors of metabolic syndrome (6, 7) have been extensively studied in adults, comparatively little emphasis has been laid on its prevalence in children and adolescents, such that there is no clear definition for the metabolic syndrome in this age group, and studies are needed in children and adolescents to better define the metabolic syndrome. Based on limited reports in this field, 4.2% of American adolescents who participated in the National Health and Nutrition Examination Study (NHANES) III had metabolic syndrome (8), a proportion that increased to 6.2% in NHANES 1999–2000 (9). Metabolic syndrome is largely confined to overweight adolescents, such that 29% of overweight adolescents (BMI ≥95th percentile for age and sex) in NHANES III (8) and 32% in NHANES 1999–2000 had this phenotype (9). As childhood overweight increases (10), it is likely that the prevalence of metabolic syndrome in this age category will increase worldwide.

The prevalence of overweight (defined as BMI ≥85th percentile for age and sex) in Tehranian adolescents has been reported to be high, with an estimated prevalence of 21% (11). Although the prevalence of the metabolic syndrome in American (8, 9, 12, 13) and Mexican (14) adolescents has been reported recently, there is no report in the present literature regarding the prevalence of this phenotype in adolescents in Middle Eastern countries. This study, therefore, was undertaken to determine the prevalence of the metabolic syndrome in an urban population of Iranian adolescents.

Research Methods and Procedures

Subjects

This study was conducted within the framework of the Tehran Lipid and Glucose Study (TLGS), a prospective study performed on a representative sample of residents of District 13 of Tehran with the aim of determining the prevalence of non-communicable-disease risk factors and developing a healthy lifestyle to improve these risk factors (15). The TLGS provides a representative sample of the urban population of Tehran (15). More than 15, 000 people ≥3 years of age living in District 13 of Tehran were selected by the multistage cluster random sampling method, including 3265 adolescents 10 to 19 years of age. In this population-based cross-sectional study, after excluding subjects taking medications that would affect serum lipids, blood pressure, and carbohydrate metabolism (n = 23), 3036 adolescents (1413 boys and 1623 girls) with full relevant data (206 adolescents had incomplete relevant data) were included. The proposal for this study was approved by the research council of the Endocrine Research Center of Shaheed Beheshti University of Medical Sciences, and informed written consent was obtained from each subject.

Methods

Details of the TLGS protocol and all laboratory procedures have been published elsewhere (3, 6, 15). Briefly, weight was measured while the subjects were minimally clothed without shoes using digital scales and recorded to the nearest 100 g. Height was measured in a standing position, without shoes, using a tape measure while the shoulders were in a normal position. BMI was calculated as weight in kilograms divided by height in meters squared. Waist circumference was measured at the narrowest level over light clothing, using an unstretched tape measure, without any pressure to body surface, and measurements were recorded to the nearest 0.1 cm. To reduce subjective error, all measurements were taken by the same person. Data on family history of diabetes were collected from the subjects’ oral responses to the pretested questionnaire. The criterion for family history of diabetes was having at least one first-degree relative with a diagnosis of diabetes after 30 years of age. A qualified physician measured blood pressure two times with the subject in a seated position during physical examinations after one initial measurement for determining peak inflation level using a standard mercury sphygmomanometer. The mean of two measurements was considered to be the participant's blood pressure. The systolic blood pressure was defined as the appearance of the first sound (Korotkoff phase 1), and diastolic blood pressure was defined as the disappearance of the sound (Korotkoff phase 5) during deflation of the cuff at a 2- to 3-mm/s decrement rate of the mercury column.

Fasting blood samples for the measurement of glucose and lipid concentrations were drawn after the subjects had fasted overnight (3). Fasting plasma glucose (FPG) was measured on the day of blood collection by the enzymatic colorimetric method using glucose oxidase. Serum total cholesterol and triglyceride (TG) concentrations were measured by commercially available enzymatic reagents (Pars Azmoon, Tehran, Iran) adapted to a Selectra autoanalyzer. High-density lipoprotein-cholesterol (HDL-C) was measured after precipitation of the apolipoprotein B—containing lipoproteins with phosphotungistic acid. Low-density lipoprotein-cholesterol was calculated from serum total cholesterol, TG, and HDL-C, except when TG concentration was >400 mg/dL.

Definition of the Components of the Metabolic Syndrome

To allow for valid cross-study comparisons, we used the age-modified standards of the ATP III metabolic syndrome criteria published previously (9, 12). Subjects with three or more characteristics of the following components were categorized as having metabolic syndrome: 1) abdominal obesity (waist circumference ≥ the age- and sex-specific 90th percentile for this population); 2) elevated blood pressure (systolic and/or diastolic blood pressure ≥ the age-, sex-, and height-specific 90th percentile, except for those 18 and 19 years old for whom the cut-off values of ≥130 and ≥85 mm Hg for systolic and diastolic blood pressure, respectively, were used instead); 3) low HDL-C level (≤40 mg/dL = 1.03 mM); 4) elevated serum TGs (≥110 mg/dL = 1.24 mM); 5) elevated FPG (≥110 mg/dL = ≥6.1 mM).

Overweight was defined based on the standardized percentile curves of BMI suggested for Iranian children and adolescents as ≥95th percentile of BMI for age and sex (16). At risk for overweight was defined as ≥85th to <95th percentile of BMI for age and sex, and normal weight was defined as <85th percentile of BMI for age and sex. For sake of cross-study comparisons, we also used Centers for Disease Control and Prevention 2000 (17) and International Obesity Task Force cut-off points (18) to define “at risk for overweight” and “overweight” adolescents. To use uniform terminology throughout the paper, we replaced the International Obesity Task Force terms of “overweight” and “obesity” by “at risk for overweight” and “overweight,” respectively.

Statistical Methods

All data were analyzed by SPSS (Version 9.09; SPSS, Chicago, IL). The prevalence of the metabolic syndrome and 95% confidence interval was calculated overall, by sex, by sex and family history of diabetes, and by sex and BMI status. The prevalence of metabolic abnormalities across categories of sex, family history of diabetes (yes or no), and BMI status (normal, at risk, overweight) was also calculated. Prevalence values were compared using the χ2 test for adolescents with and without the metabolic syndrome. We also used multivariate logistic regression analysis to determine the potential determinants of the metabolic syndrome. Statistical significance was established at p < 0.05.

Results

In our population, roughly 31.1% of subjects had no risks, 68.9% of subjects had one or more risk factors, nearly 34% had two or more risk factors, and 10.1% had the metabolic syndrome (three or more risk factors). There was no difference in the prevalence of the metabolic syndrome between boys and girls. The syndrome was more common in adolescents with a family history of diabetes than in those without a family history of diabetes. When examined by BMI category (different definitions), overweight adolescents had a higher prevalence than at-risk-for-overweight and normal-weight adolescents (Table 1).

Table 1. . Prevalence of the metabolic syndrome among Iranian adolescents*
 No. of subjectsPercent of subjects with metabolic syndromep
  • HDL-C, high-density lipoprotein cholesterol; TG, triglyceride; FPG, fasting plasma glucose; IOTF, International Obesity Task Force; CDC, Centers for Disease Control and Prevention.

  • *

    Metabolic syndrome was defined as at least three of the following: 1) abdominal obesity (waist circumference ≥90th percentile for age and sex); 2) elevated systolic or diastolic blood pressure (≥90th percentile for age, sex, and height) if age <18 years and ≥130 or ≥85 mm Hg if age ≥18 years; 3) low HDL-C (≤40 mg/dL); 4) high serum TGs (≥110 mg/dL); 5) elevated FPG (≥110 mg/dL).

  • Using Iranian cut-off points.

  • Using IOTF cut-off points.

  • §

    Using CDC2000 cut-off points.

Total303610.1 (9.0 to 11.1) 
Sex  0.76
 Male141310.3 (8.6 to 11.8) 
 Female16239.9 (8.4 to 11.3) 
Family history of diabetes  0.04
 Yes35813.1 (9.6 to 16.6) 
 No26789.7 (8.5 to 10.7) 
BMI status (percentile)  0.001
 Normal (<85th)22554.1 (3.2 to 4.8) 
 At risk (85th to <95th)39913.5 (10.1 to 16.9) 
 Overweight (≥95th)38241.9 (36.9 to 46.8) 
BMI status  0.001
 Normal24154.3 (3.5 to 5.2) 
 At risk47523.7 (19.9 to 27.6) 
 Overweight14659.5 (51.5 to 67.6) 
BMI status (percentile)§  0.001
 Normal (<85th)24574.8 (3.3 to 6.3) 
 At risk (85th to <95th)38320.1 (16.0 to 24.1) 
 Overweight (≥95th)19656.6 (49.6 to 63.6) 

When the variables were simultaneously entered into the logistic regression models, girls had higher chances than boys (1.34; 1.03 to 1.76; p < 0.05) of having metabolic syndrome, and overweight (17.8; 13.2 to 24.0; p < 0.01) and at-risk-for-overweight adolescents (3.67; 2.57 to 5.23; p < 0.01) had higher chances of having metabolic syndrome than normal-weight adolescents, but no significant association between a family history of diabetes and metabolic syndrome in adolescence was seen (1.08; 0.74 to 1.57).

The distribution of the individual components of the metabolic syndrome is shown in Table 2. Overall, low serum HDL-C and high serum TGs were the most common, whereas high FPG was the least common. Subjects with a family history of diabetes had a higher rate of abdominal obesity, low serum HDL-C, and high serum TGs than subjects without a family history of diabetes. Overweight adolescents had the highest proportion of abdominal obesity, elevated blood pressure, and high serum TGs.

Table 2. . Prevalence of individual components of the metabolic syndrome among Iranian adolescents
 Individual risk factors*
 Abdominal obesityElevated blood pressureHigh glucoseLow HDL-CHigh TGs
  • HDL-C, high-density lipoprotein cholesterol; TG, triglyceride; FPG, fasting plasma glucose.

  • *

    Abdominal obesity; waist circumference ≥90th percentile for age and sex; elevated blood pressure, systolic or diastolic blood pressure ≥90th percentile for age, sex, and height if age <18 years and ≥130 or ≥85 mmHg if age ≥18 years; low HDL-C, ≤40 mg/dL; high serum TGs, ≥110 mg/dL; elevated FPG, ≥110 mg/dL.

  • p < 0.05 compared with subjects without family history of diabetes.

  • p < 0.01 compared with subjects without family history of diabetes.

  • §

    p < 0.001 compared with normal-weight and at-risk-for-overweight subjects.

Total10.0 (9.0 to 11.1)23.8 (22.3 to 25.3)0.6 (0.3 to 0.9)42.8 (41.1 to 44.6)37.5 (35.8 to 39.3)
Sex     
 Male10.0 (8.4 to 11.6)24.1 (21.9 to 26.3)0.8 (0.3 to 1.3)44.0 (41.4 to 46.6)36.0 (33.5 to 38.5)
 Female10.1 (8.6 to 11.5)23.5 (21.4 to 25.6)0.5 (0.1 to 0.9)41.9 (39.4 to 44.3)38.9 (36.5 to 41.3)
Family history of diabetes     
 Yes12.8 (9.3 to 16.3)24.5 (20.1 to 29.0)1.6 (0.3 to 3.0)50.2 (45.0 to 55.4)40.5 (35.3 to 45.6)
 No9.7 (8.5 to 10.8)23.7 (22.1 to 25.3)0.5 (0.2 to 0.8)41.9 (40.0 to 43.7)37.1 (35.3 to 39.0)
BMI status (Iranian cut-off points)     
 Normal (<85th percentile)1.6 (1.1 to 2.1)20.0 (18.3 to 21.6)0.5 (0.2 to 0.8)38.7 (36.7 to 40.7)30.9 (29.0 to 32.8)
 At risk (85th to <95th percentile)12.5 (9.2 to 15.7)27.5 (23.1 to 31.9)1.0 (0.02 to 1.9)52.8 (47.9 to 57.8)50.6 (45.7 to 55.5)
 Overweight (≥95th percentile)57.3 (52.3 to 62.3)§42.4 (37.4 to 47.3)§1.3 (0.1 to 2.4)56.8 (51.8 to 6.18)§63.0 (58.2 to 67.9)§

Discussion

This study, conducted on an urban population of Tehran, showed a high prevalence of the metabolic syndrome among Iranian adolescents. This is the first study reporting the prevalence of the metabolic syndrome among adolescents in Middle Eastern countries and in Iran. Approximately 10% of all adolescents and nearly 42% of overweight adolescents met the criteria for this syndrome, suggesting that 1 in 10 adolescents is affected. Furthermore, more than two-thirds of all adolescents had at least one metabolic abnormality. Relatively little is known about the precise causes of such a high prevalence. This may have been the result of greater improvements in the diets of the Iranian population and a greater reduction in physical activity (19). Type of definition of metabolic syndrome and cut-off points used could also explain, to some extent, such a high prevalence.

There are only a few studies that have investigated the prevalence of metabolic syndrome in adolescents (8, 9, 12, 13, 14). Duncan et al. (9) and Cook et al. (12) used the age-modified standards of the ATP III metabolic syndrome criteria to determine the prevalence of metabolic syndrome in American adolescents. The prevalence of this syndrome that we found in this study is higher than that reported by Duncan et al. (9) and Cook et al. (12) for American adolescents. de Ferranti et al. (8), using the modified definition of the ATP III, reported the prevalence of metabolic syndrome in American adolescents to be 9.2%, ∼1% lower than this study found. Investigators from Mexico reported the prevalence of the metabolic syndrome in Mexican adolescents (12 to 19 years of age) to be 6.5% by ATP III definition and 4.5% by World Health Organization definition (14). The lack of a standard definition for the metabolic syndrome in adolescents is unfortunate and makes comparison with other studies difficult.

In this study, metabolic syndrome was more common in overweight adolescents. Previous studies also reported a high prevalence of this syndrome among overweight adolescents compared with those at risk for overweight or those with normal weight (9, 12). Overweight has important implications for the future health of adolescents. Several studies have found that child and adolescent obesity continues into adulthood and also predicts the metabolic syndrome in adults (20, 21). Therefore, there is an urgent need to develop prevention programs aimed toward childhood obesity. Although developing such programs in communities presents numerous challenges, we feel there are also many areas of strength on which to build health behavior change programs (22).

Our findings should be interpreted while considering some limitations. The major limitation of this study is the definition of metabolic syndrome; limitations of such a definition for adolescents have been discussed previously (12). We have not used the definition made by Weiss et al. (13) in this study, because all of their subjects were obese; our study, however, is a population-based study that includes both obese and non-obese adolescents. The cross-sectional nature of our study does not allow us to make causal inferences. We used waist circumference in the definition of the metabolic syndrome. Waist circumference is a more practical indicator of visceral adiposity than abdominal computed tomography or magnetic resonance imaging. However, fat distribution is affected by puberty. We attempted to control for this using age- and sex-specific waist circumference percentiles. Our results in this study are based on data from the first phase of TLGS, collected nearly 5 years ago. Because overweight has become more common now than 5 years ago in children and adolescents (23), metabolic syndrome may have a higher prevalence now than it did during the first phase of TLGS.

Our study provides evidence showing a high prevalence of the metabolic syndrome in Iranian adolescents, particularly among overweight adolescents. Similar studies should be conducted in Asian countries. Further study could better show the pathophysiology of metabolic syndrome in adolescents and its relationship to other chronic diseases.

Acknowledgement

This study was supported by National Research Council of the Islamic Republic of Iran Grant 121 and by the combined support of the National Research Council of Islamic Republic of Iran and the Endocrine Research Center of Shaheed Beheshti University of Medical Sciences. We thank the participants of the Tehran Lipid and Glucose Study for enthusiastic support and the staff of the Endocrine Research Center, Tehran Lipid and Glucose Study Unit, for valuable help in conducting this study.

Footnotes

  • 1

    Nonstandard abbreviations: ATP III, Adult Treatment Panel III; NHANES, National Health and Nutrition Examination Study; TLGS, Tehran Lipid and Glucose Study; FPG, fasting plasma glucose; TG, triglyceride; HDL-C, high-density lipoprotein-cholesterol.

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