Pediatrics International (2006) 48, 566571

doi: 10.1111/j.1442-200X.2006.02273.x

Original Article

Obesity and associated cardiovascular risk factors in Iranian children: A cross-sectional study
ANAHITA HAMIDI, HOSSEIN FAKHRZADEH, ALIREZA MOAYYERI, RASSUL POUREBRAHIM, RAMIN HESHMAT, MASOUMEH NOORI, YALDA REZAEIKHAH AND BAGHER LARIJANI Endocrinology and Metabolism Research Center, Doctor Shariati Hospital, Tehran University of Medical Science, Tehran, Iran
Abstract Background: Obesity is a growing public health problem in developing countries considering its association with cardiovascular risk factors. Relationship between childhood obesity and these risk factors has not been attested in the Iranian population before. The aim of the present study was to investigate frequency of cardiovascular risk factors and their association with severity of obesity in a sample of Iranian obese children. Methods: A total of 13 086 children aged 712 years were screened and those with waist circumference = 90th percentile of their age were invited for further evaluations. Participants were divided into two groups of overweight or obese according to International Obesity Task Force criteria. Cardiovascular risk factors were dened as high fasting total cholesterol, high low density lipoprotein, low high density lipoprotein, high triglycerides, and systolic or diastolic hypertension. These factors were compared between obese and overweight children and their correlations with body mass index and other measures of obesity were tested. Results: Of 532 children (274 boys, mean age 9.5 1.3) enrolled in the study, 194 were overweight and 338 were obese. Mean levels of triglyceride and Apo-lipoprotein B in obese children were signicantly higher than overweight participants. A total of 81.9% of obese children and 75.4% of overweight children had at least one cardiovascular risk factor. There were signicant correlations between body mass index and systolic blood pressure, diastolic blood pressure, serum triglyceride, and Apo-lipoprotein B levels (P values <0.01). Conclusion: The high prevalence of cardiovascular risk factors in overweight and obese children and positive correlation of these factors with severity of obesity emphasizes the need for prevention and control of childhood obesity from early stages. cardiovascular risk factors, childhood obesity, dyslipidemia, hypertension, prevention.

Key words

Obesity is a growing global epidemic affecting all age groups. It is currently regarded as the leading cause of preventable death worldwide and escalating obesity would be the greatest health threat the world will face in the twenty-rst century.1,2 Childhood obesity has also become a major global health concern in recent decades.3 It is associated with increasing risk of atherosclerosis, hyperinsulinemia, hypertension and psychosocial problems in the affected population.4 The prevalence of obesity among children appears to be rising rapidly in developing countries, which could be attributed to changes in lifestyle.5 Based on the data of the World

Correspondence: Professor Bagher Larijani, Endocrinology and Metabolism Research Center, Doctor Shariati Hospital, North Kargar Avenue, Tehran 14114, Iran. Email: emrc@sina.tums.ac.ir Received 13 March 2005; revised 25 June 2005; accepted 2 September 2005.

Health Organization Monica Project, over 30% of the people in the Middle East are overweight.6 A survey on secondary school students in Bahrain revealed that 15.6% of boys and 14.7% of girls were overweight.7 Like many other countries, the trend for obesity in Iranian children has doubled between 1993 and 1999.5 Even in childhood, obesity accompanies other risk factors for future cardiovascular diseases (CVD), including hypertension and dyslipidemia. This set of risk factors has been proved to accelerate progression of atherosclerotic lesions in the coronary arteries of young people.8 Obese children are at increased risk for adult mortality and morbidity particularly from CVD.9 Limited number of studies have been performed on childhood obesity and accompanying cardiovascular risk factors in the developing world. For a better understanding on the issue and more efcient programs for worldwide prevention of CVD mortality, more ethnic-specic studies are needed.

Obesity and cardiovascular risk factors

Moreover, the relationship between obesity and other newly suggested CVD risk factors (such as Apo-lipoprotein A and B) is unconrmed so far. We aimed in this study to determine frequency and assortment of these factors and their relation with severity of obesity in a sample of primary school Iranian obese children.

567

Methods
This cross-sectional study was conducted from January to May 2004 in the sixth district of Tehran. We screened 13 089 pupils aged 712 years in all of the 65 primary schools of this area. Waist circumference was used as the screening tool to nd obese children.10,11 Those with a waist circumference equal or greater than 90th percentile for their ages were invited for further evaluations. A total of 1644 students had high waist circumference, of whom 563 subjects attended a school-based clinic and enrolled in the study. The study protocol was approved by the ethics committee of Tehran University of Medical Sciences, Tehran, Iran, and written informed consent was obtained from students and their parents. Bodyweight was recorded to the nearest 0.5 kilogram (kg) using a standard beam balance scale with the subject barefoot and wearing light dresses. Body height was recorded to the nearest 0.5 centimeters (cm) according to the following protocol: no shoes, heels together and head touching the ruler with line of sight aligned horizontally. Body Mass Index (BMI) was calculated as the ratio of body weight (kg) to body height (m) squared. Participants were classied as normal, overweight or obese using the international age and gender specic BMI cut-offs recommended by the International Obesity Task Force (IOTF).12 In total, 31 students (5%) were normal weight and excluded from the analyses. Waist circumference was measured to the nearest centimeter with elastic-band meter with the student in the standing position at the level of the distal third of the distance from the xyphoid process to the umbilicus. Hip circumference was measured 4 cm below the anterior superior iliac spine and waist-to-hip ratios (WHR) were calculated as an index of abdominal obesity. One experienced physician measured blood pressure using a mercury sphyngmomanometer with a cuff size suitable for each subject. Systolic blood pressure (Korotkoff phase I) and diastolic blood pressure (Korotkoff phase V) were measured twice with a 5 min interval from the right arm in supine position and the average of the two measurements was taken as the students blood pressure. We used recommendations of Task Force for High Blood Pressure in Children and Adolescents to dene systolic or diastolic hypertension.13 Overnight fasting venous blood samples were taken from the children. Triglyceride and cholesterol levels were measured through calorimetric assays (Pars Azmoon kit, Tehran,

Iran) using automatic serum auto analyzer (Hitachi 902; Boehringer Manneheim, Germany). Low Density Lipoprotein (LDL) cholesterol, High Density Lipoprotein (HDL) cholesterol, Apo-lipoprotein A, and Apo-lipoprotein B levels were measured directly by Immunoturbidometric assay (Pars Azmoon kit; Tehran, Iran). As there is scarce evidence in hand about the borderline cholesterol levels to be considered as normal or risky for children, and considering that all of our participants were obese and at-risk children, cut-offs proposed as acceptable by the expert panel of National Cholesterol Education Program on blood cholesterol in children and adolescents were used to dene normal values.14 Total cholesterol = 170 mg/dL, LDL =110 mg/dL, HDL < 35 mg/dL, and triglyceride levels = 150 mg/dL were considered as cardiovascular risk factors. These four lipid prole variables and systolic and diastolic hypertension comprised six study target variables. The crude values of Apo-lipoproteins A and B were also entered into analyses. Pearson correlation test was used to assess the relationships between anthropometric measurements and cardiovascular risk factors. To control for the possible effects of age and height on the relationship between BMI and hypertension, partial correlation analysis was used. Differences between two groups of obese and overweight children were investigated using independent samples t-test and 2-test. Concerning necessity of type I error correction for multiple tests used in this study, P values <0.01 were considered as signicant.

Results
In total, 532 children (274 boys, mean age 9.5 1.3) were enrolled in the study. According to IOTF criteria, 194 participants were overweight and the other 338 were obese. Anthropometric measurements, blood pressures, and lipid proles of the study population are summarized in Table 1. Mean levels of triglyceride in obese children were signicantly higher than overweight group (160.3 46.0 vs 145.0 36.0, P < 0.001). Difference between the two groups regarding Apo-lipoprotein B was marginally signicant (P = 0.009). As indicated in Table 2, the percentage of participants with any of the given risk factors was higher in the obese group. The difference between two groups reached a statistical signicance level only for hypertriglyceridemia (P = 0.003). A total of 18.1% of obese children and 24.6% of overweight children had no cardiovascular risk factor. A total of 12.9% of obese children had four or ve risk factors, while this gure was 8.3% for overweight children. The percentages of participants with different numbers of risk factors are schematically presented in Figures 1 and 2 for different genders. Difference between boys and girls for none of the risk factors was signicant. As shown in Table 3, different obesity scales were highly correlated with each other. This statement was also correct for

568 A Hamidi et al.

Table 1 Physical and paraclinical characteristics of studied children Overweight Girls (n = 104) 21.8 1.7 67.7 5.3 79.6 9.7 0.82 0.04 136.6 8.1 102.6 11.2 71.2 8.5 145.8 33.0 171.1 27.4 96.8 19.6 54.7 12.3 142.1 21.2 87.3 19.4 Obese Boys (n = 184) 26.4 3.0 77.8 7.4 89.3 7.4 0.87 0.05 138.3 9.1 107.4 11.8 72.5 9.5 163.7 50.3 174.8 30.3 98.7 20.3 53.0 12.2 143.0 21.9 93.0 21.3 Girls (n = 154) 26.3 3.3 74.9 7.1 88.5 9.3 0.88 0.05 137.0 9.7 104.0 10.9 71.8 8.5 160.0 39.6 171.6 32.5 97.7 21 53.1 14.3 139.6 25.5 90.0 21.3

Boys (n = 90) Body Mass Index (kg/m ) Waist Circumference (cm) Hip Circumference (cm) Waist/hip ratio Child Height (cm) Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Triglycerides (mg/dlL) Total cholesterol (mg/dlL) LDL cholesterol (mg/dlL) HDL cholesterol (mg/dlL) Apo-lipoprotein A (mg/dlL) Apo-lipoprotein B (mg/dlL)
2

22.5 1.4 72.3 5.8 84.3 5.2 0.85 0.04 140.8 8.4 104.6 11.0 70.7 8.5 144.1 39.3 167.1 26.4 94.4 17.7 52.4 15.7 144.2 26.5 86.5 17.1

Data are presented as mean standard deviation. HDL, High Density Lipoprotein; LDL, Low Density Lipoprotein.

systolic and diastolic blood pressures as well as different components of lipid prole. Correlations between elements of lipid prole and obesity scales reached to statistical signicance only for triglyceride and Apo-lipoprotein B (Table 3). Systolic and diastolic blood pressures were signicantly correlated with anthropometric variables. The correlation between Systolic blood pressure and BMI (r = 0.297, P < 0.001) remained signicant after controlling for age (r = 0.240, P < 0.001) and height (r = 0.229, P < 0.001). Partial correlation analysis also showed an independent relationship between diastolic blood pressure and BMI controlling for age (r = 0.193, P < 0.001) and height (r = 0.199, P < 0.001).

Discussion
This is the rst study in Iran trying to explicate characteristics of obese children and to search for relationships between

severity of obesity and different cardiovascular risk factors. We observed that about 80% of our obese children are suffering from at least one established cardiovascular risk factor and these risk factors are interconnected with the severity of obesity. We found signicant correlation between crude measures of obesity (including BMI, waist circumference, and WHR) and systolic and diastolic blood pressures of children. However, the only elements of lipid prole that showed a signicant correlation with obesity measures were serum triglycerides and Apo-lipoprotein B. This could have some applications for risk assessment of CVD in children and adolescents. The results of our study are consistent with other major studies that have examined the relationship between obesity and cardiovascular risk factors in children and adolescents.9,1522 The high prevalence of hypertension in this study is in concordance with the results of other studies indicating a strong relationship between obesity and hypertension in children.16,17 The signicant and independent association between BMI and

Table 2 factors

Number of participants with different cardiovascular risk

35 30 25

Overweight Triglycerides = 150 mg/dL Total Cholesterol = 170 mg/dL LDL Cholesterol = 110 mg/dL HDL Cholesterol < 35 mg/dL Systolic Hypertension Diastolic Hypertension

Obese 162 (51.3) 145 (46.6) 87 (27.5) 8 (2.5) 76 (22.8) 121 (36.3)

P value 0.003 0.396 0.136 0.677 0.023 0.154

71 (37.6) 79 (42.7) 41 (21.6) 6 (3.2) 28 (14.6) 58 (30.2)

20 15 10 5 0 0 1 2 3 4 5

Overweight Obese

Data are presented as frequency (percentage in parentheses). Dened according to Task Force for High Blood Pressure in Children and Adolescents. HDL, High Density Lipoprotein; LDL, Low Density Lipoprotein.

Fig. 1 Distribution of boys with different numbers of cardiovascular risk factors.

Obesity and cardiovascular risk factors

Apo-lipoprotein A
35 30 25 20 15 10 5 0 1 2 3 4 5 Overweight Obese

569

Cholesterol

blood pressure (controlling for both child age and height) supports the hypothesis that early-onset obesity is accompanied by many health risks including hypertension.18 We found a signicant association between BMI and triglyceride levels in overweight or obese children. This was not true for the association of BMI with total cholesterol and LDL. Li et al. have also found that degree of obesity has no strong correlation with total cholesterol and LDL.19 Only 2.8% of the children showed low HDL levels and there was no signicant relationship between HDL and anthropometric variables in this study, which supports the hypothesis that reduced HDL level may require years of history of obesity to develop and the degree of obesity would affect HDL levels later in life.19,20 However, there was a signicant relationship between BMI and Apo-lipoprotein B levels in our sample. These ndings support the idea that measurement of the Apolipoprotein B levels is a useful initial approach to cardiovascular risk assessment in obese children.21 In contrast, we found no association between BMI and Apo-lipoprotein A levels which is similar to the ndings of other studies on obese children.22 According to some authors, reduced Apo-lipoprotein A and increased Apo-lipoprotein B levels have a strong correlation with the development and progression of Atherosclerosis, more so than their equivalent lipoproteins HDL and LDL and in children these changes are associated with the presence of CVD in their parents.23,24 Given the more uctuating and unreliable nature of triglyceride levels, Apo-lipoprotein B could be the best choice for assessment of dyslipidemia and cardiovascular risk in obese children. It has been suggested that both fat mass and fat distribution are important factors in assessing cardiovascular risk even in children.10,25 However, the lack of correlation between WHR and dyslipidemia of obese children in our study could be interpreted as this index may be less appropriate for evaluation of cardiovascular risk in children and adolescents than in adults. We also found no association between hip circumference and dyslipidemia in this study. This is similar to the results of the Bogalusa Heart Study, which emphasizes that

Triglycerides

0.413** 0.129* 0.341** 0.046 0.528** Body Mass Index (kg/m2) Waist Circumference (cm) Hip Circumference (cm) Waist/Hip ratio Systolic Blood Pressure (mmHg) Diastolic Blood Pressure (mmHg) Triglycerides (mg/dL) Total Cholesterol (mg/dL) HDL Cholesterol (mg/dL) LDL Cholesterol (mg/dL) Apo-lipoprotein A (mg/dL) Apo-lipoprotein B (mg/dL) 0.798** 0.777** 0.043 0.297** 0.236** 0.237** 0.065 0.022 0.048 0.060 0.107* 0.755** 0.027 0.383** 0.259** 0.299** 0.061 0.057 0.079 0.28 0.137* 0.413** 0.301** 0.219** 0.154** 0.047 0.075 0.062 0.070 0.021 0.052 0.007 0.038 0.096 0.083 0.110 0.067 0.095 0.463** 0.137* 0.048 0.010 0.090 0.014 0.102 0.060 0.056 0.005 0.055 0.122* 0.104

0.780** 0.896** 0.251** 0.877** *Indicates signicant correlations at the level of 0.01.**Indicates signicant correlations at the level of 0.001. BMI, Body Mass Index; BP, blood pressure; HDL, High Density Lipoprotein; LDL, Low Density Lipoprotein.

Fig. 2 Distribution of girls with different numbers of cardiovascular risk factors.

Correlation matrix of study variables for the whole study population

Table 3

BMI

Waist

Hip

Waist/Hip ratio

Systolic BP

Diastolic BP

HDL

0.612** 0.452** 0.120* 0.532** 0.906**

LDL

0.032

570 A Hamidi et al.

the hip circumference provides little information on cardiovascular risk factors in children.25 The high degree of association between waist circumference and triglycerides, Apo-lipoprotein B and blood pressure in this study is in agreement with the results of other studies which suggested that waist circumference may be better measures of fat distribution in children.25 A combination of major cardiovascular risk factors (including hypercholesterolemia, hypertriglyceridemia, and hypertension) as well as insulin resistance are now known as metabolic syndrome.26 Studies on prevalence and characteristics of this syndrome in children and adolescents also have shown similar results to this study. It has been indicated that the prevalence of metabolic syndrome increases signicantly in relation with bodyweight and severity of obesity.27,28 The main limitation of our study was the poor response rate, as from 1644 invited students only 563 (34%) participated in the study. The primary reason for nonparticipation could be the necessity of blood sampling in our study, which decreases the compliance of children. As just about one-third of invited children attended the clinic, we should be cautious to generalize obvious characteristics of these children to the Iranian obese children, however, the paraclinical nature of cardiovascular risk factors assessed in this study decreases the impact of potential selection bias on our ndings. Number of obese participants was notably higher than overweight children in our sample, however, this could not be the same as the distribution of these children across the community. Two potential explanations for this observation could be, rst, the more anxiety and apprehension of parents of more obese children regarding health status of their children (which forced them to attend with their children to the clinic), and second, the method of screening used in this study. We used the cut-off of 90th percentile for waist circumference to nd obese children. This approach seemed to be highly sensitive (as 95% of our participants were obese or overweight), but the specicity of this screening method is questionable and some overweight children might be missed. Another point is that, although most of the attended children were overweight or obese, a minority of 5% were in the normal range of weight according to IOTF criteria. Given the low number of these children and considering our purpose to nd relationships between various risk factors and severity of obesity, we excluded these children from the study. It is also of interest to evaluate the relationship between nutritional and biochemical markers and severity of obesity, which was behind the scope of this article. Further studies in this regard are warranted. The high percentage of obese children with two or more cardiovascular risk factors (55.2%) supports the notion that excess adiposity is related to a poor cardiovascular risk prole even in children. Given the growing rate of obese children in urbanizing communities like Iran, identication and management of obese children is a critical issue for health policymakers and health-care professionals to prevent progression of cardiovascular disease in the future. In summary, we detected a high prevalence of cardiovascular risk factors in overweight and obese children and positive correlation of these factors with severity of obesity. Future studies evaluating the possible role of Apo-lipoprotein B in the pathogenesis and prognosis estimation of obesity are recommended. Hypertension and dyslipidemia in overweight and obese children indicate a serious health risk and emphasize the importance of prevention and control of obesity from early childhood to improve present and future health status.

Acknowledgments
The authors are thankful to Mr. Peyman Shooshtarizadeh in the laboratory of Endocrine and Metabolism Research Center. They also appreciate the support from the Ministry of Education, Bureau of Tehran, and the pupils of the primary schools in the sixth district of Tehran for their collaboration.

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