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Volume 2012 (2012), Article ID 804643, 6 pages
Gender Differences Time Trends for Metabolic Syndrome and Its Components among Tehranian Children and Adolescents
1Obesity Research Center, Research Institute for Endocrine Science, Shahid Beheshti University of Medical Sciences, 1985717413 Tehran, Iran
2Endocrine Research Center, Research Institute for Endocrine Science, Shahid Beheshti University of Medical Sciences, 1985717413 Tehran, Iran
Received 7 January 2012; Accepted 26 February 2012
Academic Editor: Roya Kelishadi
Copyright © 2012 Maryam Barzin et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Aims. To investigate the trend of metabolic syndrome and its components in Tehran children and adolescents during a median followup of 6.6 years. Methods. Data from 1999–2001 (phase I), 2002–2005 (phase II), and 2006–2008 (phase III) of the Tehran, Lipid and Glucose Study were analyzed (; age 6–18 years) for the trend of metabolic syndrome (MetS) and its components. General estimation equation (GEE) models were used to analyze this correlated data. Results. The crude prevalence of MetS for boys at baseline was 13.2%, which increased to 16.4% in the third phase. In girls, the prevalence of Mets decreased from 11.8% at baseline to 6% during followup. The odd ratios (OR) of obesity over the whole study period were raised in both sexes. The OR of abdominal obesity increased significantly in boys, but no change was observed in girls. No significant OR was observed in boys, while OR for MetS was shown to have a decreasing trend in girls during the followup. In the three time points, the ORs of MetS decreased significantly in girls but no significant difference was observed in boys. Conclusion. Inspite of increasing trend for obesity in both sexes, the trend of MetS decreased in girls and was relatively stable in boys, in Tehranian children, and adolescents.
The metabolic syndrome (MetS) is defined as a clustering of metabolic risk factors including central obesity, hyperglycemia, dyslipidemia, and hypertension . In recent decades, obesity and metabolic risk factors among children and adolescents have been much focused on several studies showing that increasing obesity and MetS in this population is associated with a number of adverse consequences in adulthood including type 2 diabetes mellitus and coronary heart disease, most likely due to overproduction of inflammatory mediators and insulin resistance [2–4].
While current estimates indicate a 2% to 9% prevalence for MetS in US adolescents , 14.1% of Iranian children have MetS based on ATP III criteria resulting from the increasing prevalence of overweight and abdominal obesity among Iranian children and adolescents [6, 7]. Previous studies also demonstrated higher triglyceride and lower HDL-C levels in Iranian adolescents compared to their American counterparts [8, 9]. This increased prevalence would necessitate the need for identifying the time trend of Mets and its components in our population. Although the prevalence and associated risk factors of MetS have been widely studied in recent decades [10–12], much less is known in regard to changes in risk factor status over a longer period of time during childhood and adolescence, particularly in developing countries like Iran.
A few studies have evaluated the tracking of MetS and its components altogether [13–17] and most of them have provided data in support of a stability of MetS and its components in their populations [13, 14, 16]. Other studies have demonstrated an increasing trend in MetS  and its individual components [18–21]. In a recent study which used three independent sets of cross-sectional data with limited sample size in Tehranian adolescents, aged 10–19 years, reported an increasing trend for obesity, abdominal obesity . Given the above-mentioned limitations in this study, we aimed to examine the trend of MetS and its components from childhood to adolescence, due a mean of 6.6 years of followup for the first time in Middle East region using general estimation equation (GEE) analysis.
2. Materials and Methods
Subjects in this study were selected from among participants of the Tehran Lipid and Glucose Study (TLGS), a prospective study conducted to determine the risk factors and outcomes for noncommunicable diseases . To summarize, 15,005 people, aged 3 years and over, residents of district-13 of Tehran underwent a baseline examination between February 1999 and August 2001. After this cross-sectional (phase 1), subjects were categorized into the cohort and intervention groups, the latter to be educated for implementation of life-style modifications. We used metabolic and anthropometric data from phases I (1999–2001), II (2002–2005), and III (2006–2008) of the TLGS. For the current study, 5439 participants, 2643 boys and 2797 girls, aged 6–18 years who had participated at least in one of three phases, were enrolled. The study was approved by the institutional ethics committee of the Research Institute for Endocrine Sciences, affiliated to Shahid Beheshti University of Medical Sciences and was conducted in accordance with the principles of the Declaration of Helsinki.
Details of the TLGS protocol and all laboratory procedures have been published elsewhere . Briefly, trained interviewers collected information, using a pretested questionnaire which included demographic data and anthropometric indices. Weight, height, and waist circumference (WC) were measured using standard protocols. Body mass index (BMI) was calculated as weight in kilograms, divided by height in meters squared. A qualified physician measured blood pressure twice with the subject in a seated position 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. Fasting blood samples for the measurement of glucose and lipid concentrations were drawn after the subjects had fasted overnight. Fasting blood glucose (FBG) was measured on the day of blood collection by the enzymatic colorimetric method using glucose oxidase. 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 phosphotungstic acid.
We used the definition based on Cook et al. work for definition of the MetS in children and adolescents . This definition is based on criteria analogous to that of the National Cholesterol Education Program Expert Panel on Detection, Evaluation and Treatment of High Blood Cholesterol in Adult Treatment Panel III ; it defines MetS as three or more of the following: fasting TG ≥ 110 mg/dL; HDL cholesterol <40 mg/dL; WC ≥ 90th percentile for age and sex, according to national reference curves ; systolic blood pressure (SBP) and/or diastolic blood pressure (DBP) ≥90th percentile for sex, age and height, from national reference cut-off points ; FBG ≥ 100 mg/dL. For the subjects who were aged over 18 years after the followup, we used the criteria for MetS in adults, specified by the Joint Interim Statement (JIS) . Obesity 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 .
2.2. Statistic Analysis
All continuous data are expressed as mean ± SD, and categorical variables are expressed as percentages. Independent t-test was used to compare difference between two sexes within in each phase. The general estimation equation (GEE) use the generalized linear model to estimate more efficient and unbiased analysis of demographic variables, anthropometric indices, and biochemical variables collected in longitudinal, nested, or repeated measures designs [28, 29]. This method relies on independence across subjects to consistently estimate the variance of the proposed estimators even when the assumed working correlation structure is incorrect. Logistic regression analysis was performed using GEE method for binominal variables. Variables were adjusted for age (years), time (phase) and intervention.
All analyses were performed using SPSS for Windows (version 16; SPSS Inc., Chicago, IL, USA), and significance was set at .
For the current study, we had 3,854, 3,057, and 3,441 observations in phases I, II, and III, respectively. The GEE analysis was performed with 5,439 subjects (2643 boys), aged 6–18 years, who had at least one observation in whole period the study. At baseline, girls had higher mean values for WC (), TG (), LDL, and cholesterol () but lower SBP and FBS than boys (). At the end of followup, all factors were higher in boys, while cholesterol and HDL values were higher in girls (, Table 1).
The crude prevalence of obesity increased in both sexes during a median follow-up of 6.6 years. Abdominal obesity increased from 12.3% to 33.1 in phase III in boys, but remained fairly stable in girls. The most frequent component of MetS was low HDL at baseline (39%) that increased up to 47% for boys and 43% for girls in the third phase. High TG was the next most prevalent component that decreased from 35% and 31% at baseline to 21% and 25% in girls and boys, respectively. The prevalence of MetS was 13.2% for boys at baseline that increased to 16.4% in the third phase. In girls, the prevalence of Mets decreased from 11.8% at baseline to 6% during followup (Figure 1).
The odds of obesity over the whole study period were raised in both sexes (). While the odds of abdominal obesity increased significantly in boys (), whereas no significant change was observed in girls ( = NS). The odds for all other MetS component values declined towards the end of followup, except for HDL in girls. At three time points, the odds of MetS decreased significantly in girls (OR: 0.69 and 0.55 in phases II and III, resp.) but no significant difference was observed in boys (OR: 1.1 and 0.94 = NS in phases II and III resp., Table 2).
Using GEE analysis, the results of present study conducted on 5,439 Tehranian children and adolescents, aged 6–18 years, suggest that during a median follow-up of 6.6 years, the trend of obesity increased in both sexes and for abdominal obesity increased almost three folds in boys. In spite of the increasing trend for the above factors, the trend for MetS decreased in girls and remained relatively stable in boys.
The high prevalence of obesity and MetS in childhood and adolescence has been shown to increase the prevalence of cardiovascular events in adults . Childhood and adolescent MetS have evolved into a worldwide epidemic, up to 14% in Australian  and 11% in Italian children . Findings from previous studies in Iran have revealed a higher prevalence of MetS among Iranian children (9.8% ) compared with western (4.2% in US ) and Asian countries (1.4% in Japan  and 1.8% in Korea  6.6% in China ). Several previous epidemiological studies demonstrated different trends for MetS and cardiometabolic risk factors among children and adolescents [13–17], which can be explained by variety in MetS definitions, length of followup, and also specific cultural and ethnical composition of studied population, lifestyle, and public health policies. In the Young Finns Study, a follow-up study of 1769 girls and 1688 boys, aged 3–18 years old, the prevalence of MetS increased with age in boys, and in 9–12 years old age girls . The results from the Quebec family study indicated that indicators of MetS are moderately stable from childhood to adolescence . Based on the Fels longitudinal study, authors concluded that 8 cardiometabolic risk factors associated with the MetS were relatively stable among children and adolescents . On the other hand, results from the Korean NHANES Survey on 4164 subjects, aged 10–19 years, demonstrated a decline in prevalence of MetS, despite an increase in obesity in Korean adolescents . In agreement with the Korean study, despite increasing trend of obesity, we found a decreasing trend of MetS in girls, but it relatively stable in boys mostly as a result of improvement in other MetS components. Similarly, an increasing prevalence of childhood obesity has been reported around the world [35–37]. Rapidly changing dietary practices and a sedentary lifestyle have led to increasing prevalence of childhood obesity (5–19 years) in developing countries recently  such as Iran . Moreover, recent systematic reviews and meta-analyses of available randomized trials reported nonsignificant effects of pharmacologic and behavioral treatments for reduction of overweight and obesity in children and adolescents [39, 40]. Regarding above mentioned studies, cardiometabolic risk factors were stable across time besides increasing trend of obesity in children and adolescents.
The decreasing prevalence of cardiometabolic risk factors can be explained by the positive effects of public health interventions in terms of lifestyle behaviors and increased physical activity on unfavorable risk factors. Accordingly, a systematic review has shown that higher physical activity levels were consistently associated with an improved metabolic profile and a reduced risk for MetS and/or insulin resistance in pediatric populations . We speculate that recent changes in physical activity in addition to national health care initiatives in Tehran may have had a positive impact on the prevalence of MetS. We also found some notable differences between genders in the trend of MetS, for which however we do not have an adequate explanation; it could possibly be explained by more focus of public educational programs on girls compared to boys, leading to decreasing trend of MetS in girls.
The strength of our study was the considerable sample size of children and adolescents with a long followup period over which we measured MetS and its components enabling us to assess the time effect of these risk factors in our population using the GEE model for the first time.
However, our study had several limitations. First, our subjects were from a homogeneous population, potentially limiting the generalizability of our results. Second, we did not have data regarding puberty status which have helped us to assess the effects of puberty on MetS, and third, we did not take into account some possible confounders such as physical activity, dietary habits, and socioeconomic status in our analysis.
In conclusion, inspite of the increasing trend for obesity in both sexes, the trend for MetS decreased in girls and remained relatively stable in boys in our population. Given the proven association between childhood and adolescence, obesity, and accuracy of cardiovascular events in adulthood, we are not sure that our observations, indicating persistency of excess weight along with reduction of cardiometabolic risk factors can be translated to decrease cardiovascular event rates in future adulthood. Further prospective studies with long-term followup are needed to answer this question.
Conflict of Interests
All the authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.
The authors thank Dr. Kelishadi for her assistance, and Mrs Shiva for language editing of the manuscript. They would like to express their appreciation to the staff of the Endocrine Research Center and especially all of the mothers and children who participated in this study.
- J. I. Cleeman, “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),” Journal of the American Medical Association, vol. 285, no. 19, pp. 2486–2497, 2001.
- J. A. Morrison, L. A. Friedman, P. Wang, and C. J. Glueck, “Metabolic syndrome in childhood predicts adult metabolic syndrome and type 2 diabetes mellitus 25 to 30 years later,” Journal of Pediatrics, vol. 152, no. 2, pp. 201–206, 2008.
- F. M. Biro and M. Wien, “Childhood obesity and adult morbidities,” American Journal of Clinical Nutrition, vol. 91, no. 5, pp. 1499S–1505S, 2010.
- K. J. Nadeau, D. M. Maahs, S. R. Daniels, and R. H. Eckel, “Childhood obesity and cardiovascular disease: links and prevention strategies,” Nature Reviews Cardiology, vol. 8, no. 9, pp. 513–525, 2011.
- S. Cook, P. Auinger, C. Li, and E. S. Ford, “Metabolic syndrome rates in United States adolescents, from the National Health and Nutrition Examination Survey, 1999–2002,” Journal of Pediatrics, vol. 152, no. 2, pp. 165–170, 2008.
- R. Kelishadi, G. Ardalan, R. Gheiratmand, K. Adeli, A. Delavari, and R. Majdzadeh, “Paediatric metabolic syndrome and associated anthropometric indices: the CASPIAN Study,” Acta Paediatrica, vol. 95, no. 12, pp. 1625–1634, 2006.
- M. Barzin, F. Hosseinpanah, S. Fekri, and F. Azizi, “Predictive value of body mass index and waist circumference for metabolic syndrome in 6-12-year-olds,” Acta Paediatrica, vol. 100, no. 5, pp. 722–727, 2011.
- F. Azizi, M. Rahmani, A. Ghanbarian et al., “Serum lipid levels in an Iranian adults population: Tehran lipid and glucose Study,” European Journal of Epidemiology, vol. 18, no. 4, pp. 311–319, 2003.
- A. Esmaillzadeh, P. Mirmiran, L. Azadbakht, A. Etemadi, and F. Azizi, “High prevalence of the metabolic syndrome in Iranian adolescents,” Obesity, vol. 14, no. 3, pp. 377–382, 2006.
- F. Azizi, P. Salehi, A. Etemadi, and S. Zahedi-Asl, “Prevalence of metabolic syndrome in an urban population: Tehran lipid and glucose Study,” Diabetes Research and Clinical Practice, vol. 61, no. 1, pp. 29–37, 2003.
- R. H. Eckel, K. G. M. M. Alberti, S. M. Grundy, and P. Z. Zimmet, “The metabolic syndrome,” The Lancet, vol. 375, no. 9710, pp. 181–183, 2010.
- E. S. Ford, W. H. Giles, and W. H. Dietz, “Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey,” Journal of the American Medical Association, vol. 287, no. 3, pp. 356–359, 2002.
- C. Li, E. S. Ford, T. T. K. Huang, S. S. Sun, and E. Goodman, “Patterns of change in cardiometabolic risk factors associated with the metabolic syndrome among children and adolescents: the Fels longitudinal Study,” Journal of Pediatrics, vol. 155, no. 3, pp. S5.e9–S5.e16, 2009.
- J. C. Eisenmann, G. J. Welk, E. E. Wickel, and S. N. Blair, “Stability of variables associated with the metabolic syndrome from adolescence to adulthood: the aerobics center longitudinal Study,” American Journal of Human Biology, vol. 16, no. 6, pp. 690–696, 2004.
- M. J. Park, B. A. Boston, M. Oh, and S. H. Jee, “Prevalence and trends of metabolic syndrome among Korean adolescents: from the Korean NHANES Survey, 1998–2005,” Journal of Pediatrics, vol. 155, no. 4, pp. 529–534, 2009.
- P. T. Katzmarzyk, L. Perusse, R. M. Malina, J. Bergeron, J. P. Despres, and C. Bouchard, “Stability of indicators of the metabolic syndrome from childhood and adolescence to young adulthood: the Quebec Family Study,” Journal of Clinical Epidemiology, vol. 54, no. 2, pp. 190–195, 2001.
- O. T. Raitakari, K. V. K. Porkka, J. S. A. Viikari, T. Ronnemaa, and H. K. Akerblom, “Clustering of risk factors for coronary heart disease in children and adolescents. The cardiovascular risk in young Finns Study,” Acta Paediatrica, vol. 83, no. 9, pp. 935–940, 1994.
- X. Chen and Y. Wang, “Tracking of blood pressure from childhood to adulthood: a systematic review and meta-regression analysis,” Circulation, vol. 117, no. 25, pp. 3171–3180, 2008.
- L. S. Webber, S. R. Srinivasan, W. A. Wattigney, and G. S. Berenson, “Tracking of serum lipids and lipoproteins from childhood to adulthood. The Bogalusa Heart Study,” American Journal of Epidemiology, vol. 133, no. 9, pp. 884–899, 1991.
- R. M. Fuentes, I. L. Notkola, S. Shemeikka, J. Tuomilehto, and A. Nissinen, “Tracking of systolic blood pressure during childhood: a 15-year follow-up population-based family study in eastern Finland,” Journal of Hypertension, vol. 20, no. 2, pp. 195–202, 2002.
- R. M. Fuentes, I. L. Notkola, S. Shemeikka, J. Tuomilehto, and A. Nissinen, “Tracking of body mass index during childhood: a 15-year prospective population-based family study in eastern Finland,” International Journal of Obesity, vol. 27, no. 6, pp. 716–721, 2003.
- F. Hosseini-Esfahani, A. Mousavi Nasl Khameneh, P. Mirmiran, A. Ghanbarian, and F. Azizi, “Trends in risk factors for cardiovascular disease among Iranian adolescents: the tehran lipid and glucose study, 1999–2008,” Journal of Epidemiology, vol. 21, no. 5, pp. 319–328, 2011.
- F. Azizi, A. Ghanbarian, A. A. Momenan et al., “Prevention of non-communicable disease in a population in nutrition transition: Tehran lipid and glucose study phase II,” Trials, vol. 10, article 5, 2009.
- S. Cook, M. Weitzman, P. Auinger, M. Nguyen, and W. H. Dietz, “Prevalence of a metabolic syndrome phenotype in adolescents: Findings from the third National Health and Nutrition Examination Survey, 1988–1994,” Archives of Pediatrics and Adolescent Medicine, vol. 157, no. 8, pp. 821–827, 2003.
- R. Kelishadi, M. M. Gouya, G. Ardalan et al., “First reference curves of waist and hip circumferences in an Asian population of youths: CASPIAN study,” Journal of Tropical Pediatrics, vol. 53, no. 3, pp. 158–164, 2007.
- R. Kelishadi, G. Ardalan, R. Gheiratmand et al., “Blood pressure and its influencing factors in a national representative sample of Iranian children and adolescents: the CASPIAN Study,” European Journal of Cardiovascular Prevention and Rehabilitation, vol. 13, no. 6, pp. 956–963, 2006.
- K. G. M. M. Alberti, R. H. Eckel, S. M. Grundy et al., “Harmonizing the metabolic syndrome: a joint interim statement of the international diabetes federation task force on epidemiology and prevention; National heart, lung, and blood institute; American heart association; World heart federation; International atherosclerosis society; and international association for the study of obesity,” Circulation, vol. 120, no. 16, pp. 1640–1645, 2009.
- S. L. Zeger and K. Y. Liang, “Longitudinal data analysis for discrete and continuous outcomes,” Biometrics, vol. 42, no. 1, pp. 121–130, 1986.
- S. L. Zeger, K. Y. Liang, and P. S. Albert, “Models for longitudinal data: a generalized estimating equation approach,” Biometrics, vol. 44, no. 4, pp. 1049–1060, 1988.
- P. W. Franks, R. L. Hanson, W. C. Knowler, M. L. Sievers, P. H. Bennett, and H. C. Looker, “Childhood obesity, other cardiovascular risk factors, and premature death,” The New England Journal of Medicine, vol. 362, no. 6, pp. 485–493, 2010.
- E. A. C. Sellers, G. R. Singh, and S. M. Sayers, “Large waist but low body mass index: the metabolic syndrome in Australian aboriginal children,” Journal of Pediatrics, vol. 153, no. 2, pp. 222–227, 2008.
- P. Di Bonito, C. Forziato, E. Sanguigno et al., “Prevalence of the metabolic syndrome using ATP-derived definitions and its relation to insulin-resistance in a cohort of Italian outpatient children,” Journal of Endocrinological Investigation, vol. 33, no. 11, pp. 806–809, 2010.
- I. Saito, M. Mori, H. Shibata, H. Hirose, M. Tsujioka, and H. Kawabe, “Prevalence of metabolic syndrome in young men in Japan,” Journal of Atherosclerosis and Thrombosis, vol. 14, no. 1, pp. 27–30, 2007.
- W. Liu, R. Lin, A. Liu, L. Du, and Q. Chen, “Prevalence and association between obesity and metabolic syndrome among Chinese elementary school children: a school-based survey,” BMC Public Health, vol. 10, article 780, 2010.
- C. L. Ogden, K. M. Flegal, M. D. Carroll, and C. L. Johnson, “Prevalence and trends in overweight among US children and adolescents, 1999–2000,” Journal of the American Medical Association, vol. 288, no. 14, pp. 1728–1732, 2002.
- S. Bjornelv, S. Lydersen, J. Holmen, T. I. Lund Nilsen, and T. L. Holmen, “Sex differences in time trends for overweight and obesity in adolescents: the Young-HUNT study,” Scandinavian Journal of Public Health, vol. 37, no. 8, pp. 881–889, 2009.
- M. L. Booth, T. Chey, M. Wake et al., “Change in the prevalence of overweight and obesity among young Australians, 1969–1997,” American Journal of Clinical Nutrition, vol. 77, no. 1, pp. 29–36, 2003.
- N. Gupta, K. Goel, P. Shah, and A. Misra, “Childhood obesity in developing countries: epidemiology, determinants, and prevention,” Endocrine Reviews, vol. 33, no. 1, pp. 48–70, 2012.
- L. McGovern, J. N. Johnson, R. Paulo et al., “Treatment of pediatric obesity: a systematic review and meta-analysis of randomized trials,” Journal of Clinical Endocrinology and Metabolism, vol. 93, no. 12, pp. 4600–4605, 2008.
- C. C. Kamath, K. S. Vickers, A. Ehrlich et al., “Behavioral interventions to prevent childhood obesity: a systematic review and metaanalyses of randomized trials,” Journal of Clinical Endocrinology and Metabolism, vol. 93, no. 12, pp. 4606–4615, 2008.
- B. C. Guinhouya, H. Samouda, D. Zitouni, C. Vilhelm, and H. Hubert, “Evidence of the influence of physical activity on the metabolic syndrome and/or on insulin resistance in pediatric populations: a systematic review,” International Journal of Pediatric Obesity, vol. 6, no. 5-6, pp. 361–388, 2011.