Original article Waist circumference in children and adolescents correlate with metabolic syndrome and fat deposits in young adults Jose Vicente Spolidoro a, *, Manoel L. Pitrez Filho b , Luiz T. Vargas b , João C. Santana b , Eduardo Pitrez c , Jorge A. Hauschild b , Neide M. Bruscato d , Emilio H. Moriguchi e , Augusto K. Medeiros f , Jefferson P. Piva g a Medical School of the Pontifícia Universidade Católica do RS, Moinhos de Vento Hospital, Porto Alegre, RS, Brazil b Medical School of the Pontifícia Universidade Católica do RS, Porto Alegre, RS, Brazil c Hospital de Clínicas de Porto Alegre, RS, Brazil d Veranópolis Longevity Project, Veranópolis County, RS, Brazil e UNISINOS University, Federal University of Rio Grande do Sul, Moinhos de Vento Hospital, Porto Alegre, RS, Brazil f Pontifícia Universidade Católica do RS, Porto Alegre, RS, Brazil g Medical School of the Pontifícia Universidade Católica do RS and Federal University of RS, Porto Alegre, RS, Brazil article info Article history: Received 27 November 2011 Accepted 31 May 2012 Keywords: Pediatrics Child Adolescent Waist circumference Abdominal fat Obesity summary Background & aims:To determine the relevance of waist circumference (WC) measurement and moni- toring in children and adolescents as an early indicator of overweight, metabolic syndrome (MS) and cardiovascular problems in young adults in comparison with visceral and subcutaneous adiposity. Methods:A cohort study with 159 subjects (51.6% female) started in 1999 with an average age of 13.2 years. In 1999, 2006 and 2008 weight, height, and WC were evaluated. In 2006 blood samples for laboratory diagnosis of MS were added. In 2008 abdominal computed tomography (ACT) to quantify the fat deposits were also added. Results:The WC measured in children and adolescents was strongly correlated with body mass index (BMI) measured simultaneously. A strong correlation was established between WC in 1999 with measures of WC and BMI as young adults. WC strongly correlated with fat deposits in ACT. The WC in 1999 expressed more subcutaneous fat (SAT), while the WC when young adults expressed strong correlation with both visceral fat (VAT) and SAT. The correlation of WC with fat deposits was stronger in females. WC and not BMI in 1999 was signi?cantly higher in the group that evolved to MS. Conclusions:The WC in children and adolescents was useful in screening patients for MS. WC expressed the accumulation of abdominal fat; especially subcutaneous fat. ?2012 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved. 1. Background & aims In recent decades the prevalence of obesity is increasing in many countries around the world. This fact is of concern because excess body fat, especially abdominal fat, is directly related to changes in lipid pro?le. It is also associated with increased blood pressure and hyperinsulinemia, which are considered risk factors for developing chronic diseases such as diabetes mellitus type 2 and cardiovas- cular diseases. However, the question now is how many of these changes are already present in obese children and adolescents. European studies on cardiovascular risk had already shown in the 80?s that abdominal obesity would be a better predictor of cardio- vascular disease than body mass index (BMI). 1 Data from the Bogalusa Heart Study allowed cutoff points of BMI and waist circumference (WC) in children and adolescents for cardiovascular disease risk. 2 Also using data from four British cohort studies (over 9000 patients), BMI and WC were good parameters to access risk of obesity and its consequences. 3 The BMI has been routinely used in clinics and as an evaluation tool in public health for decades to identify individuals and pop- ulations at risk of future cardiovascular disease and diabetes. However, in recent years, the BMI has been criticized as a measure of risk because it re?ects both fat mass and lean body mass, and because it is not possible to discriminate the distribution of fat. 4 There is a growing body of evidence suggesting that abdominal fat is more important as a risk factor for cardiovascular and metabolic disease than is general adiposity. 5 The mechanisms by which abdominal fat contributes to the risk of these diseases are not fully understood. The visceral adipose tissue is a very active metabolic element of abdom- inal fat, and probably plays a fundamental role in this process. 6 *Corresponding author. PUCRS, Pediatrics, Av. Ipiranga 6690/715, 90610000 Porto Alegre, RS, Brazil. Tel.:þ55 51 99858440; fax:þ55 51 33363533. E-mail address:jspolidoro@uol.com.br(J.V. Spolidoro). Contents lists available atSciVerse ScienceDirect Clinical Nutrition journal homepage: http://www. elsevier.com/locate/clnu 0261-5614/$esee front matter?2012 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved. http://dx.doi.org/10.1016/j.clnu.2012.05.020 Clinical Nutrition 32 (2013) 93e97 The aim of our study was to determine the importance of monitoring the measure of WC in a cohort of children and adolescents as a screening tool for metabolic syndrome (MS) in young adults. We compared WC in 1999 with the diagnostic of MS as young adults (2006) and deposits of fat in the abdominal computed tomography (ACT) scan and blood pressure in 2008. 2. Materials and methods We conducted a cohort study, longitudinal, observational, descriptive and analytical, with cross-cutting interventions. The cohort involved children and adolescents (7e18 years old) residing in Veranópolis, South of Brazil in 1999, both from urban and rural areas, with at least one parent alive. Veranópolis is a city with a population predominantly of white Caucasians, originally from Italy, Europe, internationally known for its high longevity. The sample was obtained from a representative and random choice of the age group investigated. Exclusion criteria was 1 : with a history of any chronic diseases or coagulopathy 2 ; with acute pathology, such as infectious diseases 3 ; in oral anti- coagulant therapy and oral contraceptives 4 ; pregnant or females with delayed menstruation. The study was carried out on cross-cutting assessments: (1999) personally identi?able information was collected; anthropometric data (weight, height, and WC) was collected in all three assess- ments; (2006) blood was collected for measurement of triglycer- ides, serum total cholesterol, LDL and HDL and blood glucose; (2008) ACT was also performed. All assessments were made by the same team of professionals. Standardized protocols were used to anthropometric parame- ters 7 : weight, height, WC. WC was obtained from the narrowest point between the lower edge of the cage framework and the iliac crest using a?exible tape measure, but not elastic. We calculated the Z score of height, weight, WC and BMI using reference values of mean and standard deviation for each of them by age, thus stan- dardizing the sample. 8e11 Cutoff points determined by Katzmarzyk et al. 2 were used for cardiovascular risk and the criteria for De Ferranti et al. 12 for diagnosis of MS. Abdominal CT exams were performed on the same day of the anthropometric measurement. The examinations were acquired with HiSpeed CT ? scan equipment (GE, Milawukee, USA). Patients were positioned supine with feet facing the inside of the machine, and then focused the cuts on the umbilicus. We obtained only one cut in each patient, for reducing the radiation (about 2.3 mGy per examination). The images were obtained with 120 kVp, 100 mAs, ?eld of view (FOV) of 36e40 cm, thickness 10 mm, tilt table, cut from 1 s, matrix 515512, with?lter and window to share moles. The images were acquired in DICOM 3.0 ? protocol and stored for later analysis. Data analysis was performed using manipulation by the computer program?Image J 1.45S? ? (free download at internet)?. The analyses were done by two radiologists blinded to clinical and anthropometric data of patients. Initially, the images were manipulated so that only densities between (?190) to (?30) Houns?eld units were analyzed (de?ned densities for fat by set-ups of literature. 13 It was initially designed the outer contour (abdominal perimeter), and it was calculated by the computer in mm 2 the total fat of the abdomen (TF). It was then designed the outline of the inner portion of the abdomen, following the inner edge of the interface between the muscle wall and the underlying fat. The psoas muscles were also excluded. The value obtained was termed internal or visceral fat (VAT). The difference between the values of total fat and internal fat was termed external or subcutaneous fat (SAT). 2.1. Statistical analysis Data was entered into a spreadsheet in Microsoft Of?ce Excel 2007 ? , and subsequently exported to the analysis in SPSS-18.0 ? .To compare quantitative variables with symmetrical distribution, we used the Studentttest for independent samples and those whose distribution was skewed by the ManneWhitney test. Categorical variables were associated by Chi-square test with Yates correction. Quantitative variables were correlated by Pearson correlation coef?cient. It was considered a signi?cant level of 5%. 2.2. Ethical aspects The research project was approved by the Scienti?c Committee of the Medical School, and by the Research Ethics Committee of PUCRS, Brazil, for their implementation, in accordance with Reso- lution No. 196/96 of the National Board of Health. All participants who agreed to participate in this study were required to sign the consent form at each stage in 1999, 2006 and 2008, if they were under the age of 18, consent was signed by the parents. 3. Results 159 children and adolescents were enrolled in this study. In 1999, during the?rst survey, the average age was 13.22.2 years and 51.6% were females. This and other characteristics of the pop- ulation are inTable 1. WC in 1999 showed a very strong correlation with BMI in the same year (r¼0.917,p<0.001), as well as when it was compared with BMI in 2006 and 2008 (r¼0.685,p<0.001 andr¼0.545, p<0.001 respectively). WC in 1999 showed a strong correlation with WC in 2006 and 2008 (r¼0.631,p<0.001 andr¼0.619 p<0.001 respectively). No differences were seen regarding gender. Table 1 Anthropometric and laboratory characteristics of the study population in the three times of observation. 1999 2006 2008 n¼159 n¼159 n¼159 Age, years 13.2 2.6 20.7 2.6 22.7 2.6 Sex,n(%) ee e Male 77 (48.4) ee Female 82 (51.6) ee Weight, Kg 53.3 15.3 67.6 14.6 71.1 15.6 Zweight 0.5 ( e0.1 a 1.3) 0.15 (e0.3 a 0.8) 0.36 (e0.2 a 0.9) Height, m 1.6 0.1 1.7 0.1 1.7 0.1 Zheight 0.22 ( e0.5 a 0.8)?0.12 (?0.7 a 0.4)?0.05 (e0.5 a 0.6) BMI, Kg/m 2 21.43.9 23.5 3.8 24.3 3.9 ZBMI 0.43 (0.1 a 1.3) 0.19 ( e0.3 a 0.7) 0.4 (e0.2 a 0.9) WC, cm 72.7 11.1 77.1 10.1 84.1 10.6 ZWC 0.1 ( e0.2 a 0.7)?0.55 (e1a?0.1)?0.37 (e0.9 a 0.3) VAT, cm 2 ee 52 (37 a 80) SAT, cm 2 ee 229 (146 a 319) TF, cm 2 ee 280 (190 a 397) SBP, mmHg 109.6 11 119.1 15 130.5 18 DBP, mmHg 68.1 7 72.1 13.5 78.7 13.3 HDL, mg/dL e 53.110.8 e Trigl, mg/dLe 81 (61 a 109) e Gluc, mg/dL e 87.916.5 e Data presented in meansd or median (P25 a P75); and for categorical variables n(%). Zweight¼Z score for weight; Zheight¼Z score for height; BMI¼body mass index; ZBMI¼Z score for BMI; WC¼waist circumference; ZWC¼Z score for waist circumference; VAT¼visceral fat at abdominal CT scan; SAT¼subcutaneous fat at abdominal CT scan; TF¼total fat at abdominal CT scan; SBP¼systolic blood pressure; DBP¼diastolic blood pressure; HDL¼serum HDL cholesterol; Trigl¼serum triglycerides; Gluc¼serum glucose. J.V. Spolidoro et al. / Clinical Nutrition 32 (2013) 93e9794 3.1. Fat deposits in the abdominal CT scan In 2008, 133 of 159 individuals underwent abdominal computed tomography (CT) to quantify the accumulation of fat in the abdomen. This quanti?cation was de?ned in: total abdominal fat, which was distributed in subcutaneous fat (SAT) and visceral fat (VAT). The comparison of Z score for WC in 1999 and 2006, with the accumulation of fat in the abdominal CT in 2008 showed stronger correlation with SAT (Pearson correlation with WC Z score in 2006 r¼0.622,p<0.001) (Fig. 1). The Z score for WC in 2006 in females showed a stronger correlation both for VAT and SAT in relation to male (female WC vs VATr¼0.522,p<0.001, and WC vs SAT r¼0.725,p<0.001; and males WC vs VATr¼0.249,p¼0, 46, and WC vs SATr¼0.532,p<0.001). The comparison of Z score for WC and abdominal CT fat deposits in 2008 showed strong correlation for VAT and SAT, stronger for SAT (Fig. 2). All analysis showed stronger correlations between WC and VAT and SAT in women. 3.2. Metabolic syndrome Adopting the criteria proposed by De Ferranti et al., 12 8.8% (14/ 159) of individuals in this cohort?lled the criteria for MS in 2006. Waist circumference but not BMI in 1999 correlated with diagnosis of Metabolic Syndrome in 2006 (Table 2). 4. Discussion 4.1. Main results a) The WC measurement as a child or adolescent correlates strongly with BMI measured simultaneously, and established a strong correlation with measurements of WC as young adults, as well as the evolution of BMI; b) WC correlates strongly with deposits of fat in abdominal CT, and WC as a child and adolescent best expresses the subcutaneous fat (SAT), whereas WC when young adults, both expressed strong correlation with visceral fat (VAT) and with SAT. The correlation of WC with the fat deposits was stronger in females; c) diagnosis of MS as a young adult correlates better with higher WC than BMI during childhood and adolescence. 4.2. Importance of WC WC is an excellent parameter to assess obesity. 14,15 Its measurement is easier and cheaper, requiring only a tape measure. To determine the BMI requires a weighing scale and a stadiometer. Based on our results we believe that WC can be used as a measure of population screening for obesity, as well as an element in the diagnosis of metabolic syndrome. Most individuals with increased WC remained so in the three assessments. This occurred in both sexes. Early recognition of signs of obesity, especially abdominal obesity is very important, targeting the control of its serious consequences. Fat deposits in the abdominal CT scan: the correlation of Z score for WC in all the tests was stronger with SAT. In 2008 this corre- lation occurred with both SAT and VAT. Several authors have re- ported that VAT (visceral fat) correlates more strongly with metabolic risk factors and metabolic syndrome than SAT (subcu- taneous fat). 16e18 These studies are limited, however, because in general the same patients have increased both SAT and VAT, which makes it dif?cult to distinguish the actual contribution of each one compared to the presence of signs of MS. Pou et al. 19 found increased SAT and VAT in patients with high BMI. They also showed that VAT increases with age, while SAT signi?cantly decreased among old individuals. 19 In our study, the WC clearly expressed the accumulation of abdominal fat, once again reinforcing the impor- tance of a simple anthropometric measurement for the early suspicion of MS, and its usefulness for prevention of severe complications in adulthood. We found in this cohort that waist circumference did not express a direct relationship with VAT, but as the study of Pou et al., 19 clearly expressed an increase in abdominal fat, both subcutaneous and visceral, particularly in the analysis of 2008. The progressively stronger correlation between WC and VAT in each of the three assessments can express the interference of age on visceral fat as Pou et al. reported. 19 The correlation between WC and abdominal fat distribution varies among different ethnic groups. Among blacks there is a greater accumulation of SAT in relation to BMI than whites and Asians. 20 The largest amount of VAT is related to low levels of adiponectin, which is associated with increased risk of cardiovas- cular disease. 21 We can therefore speculate that the strongest correlation between WC and SAT in this cohort, can express a characteristic of this population and may indicate a positive factor that can contribute to their longevity. Waist circumference nine years earlier already showed a strong correlation with?ndings in the abdominal CT, while in all measurements the WC better expressed the abdominal fat deposits among girls, especially in 2006 and 2008, when everyone already completed puberty. The difference between the sexes was evident, Fig. 1.Comparison of waist circumference (WC) in 1999 with visceral fat (VAT) and subcutaneous fat (SAT) in abdominal CT in 2008. [Pearson Correlation Coef?cient (r)]. J.V. Spolidoro et al. / Clinical Nutrition 32 (2013) 93e97 95 suggesting that there may be hormonal in?uences for this fatty deposition. In men, obesity is called android, with accumulation of VAT, while women?s obesity is called gynecoid, with predominance of SAT, either in abdomen as well as in thighs and buttocks. 22e24 In our series, the hip circumference was not measured. Waist circumfer- ence was not signi?cantly different between the sexes, but abdom- inal fat deposits correlate more strongly with women?s WC. This may explain why the correlation of WC was stronger with the SAT. It is recognized that VAT, more than SAT, exerts a greater in?uence on the hepatic release of free fatty acids which, in turn, has a greater effect in raising blood pressure than the brain. 25 The brain may increase blood pressure (BP) through vagal afferent signals, increasing adrenal sympathetic activity. 25,26 Hayashi et al. 27 followed a cohort of 300 subjects for 10e11 years with normal BP at the beginning. Of these, 92 developed hypertension. VAT and SAT was higher in hypertensive compared to those who remained with normal BP. We know that adipocytes of fat tissue have recognized endocrine effect, are able to synthesize and release several peptide and non peptide compounds, particularly the VAT. 28,29 Some of these, such as adipo- nectin and plasminogen activator inhibitor, have a proven relation- ship with the BP. 20,21,29,30 Adiponectin has a protective effect and its levels are inversely proportional to the amount of VAT 21 and WC. 31 Adiponectin in vitro has shown improvements in insulin function, as protection against aterosclerosis. 25 Therefore, the endocrine function adipocytes may have a key role in the risk of developing hypertension, especially, but not exclusively, associated with VAT. In a sample of children aged 10e14 years in Cyprus, 32 WC was a better predictor of cardiovascular disease risk than BMI. Those with WC above the 75th percentile had signi?cantly higher odds of having high BP, elevated total cholesterol, low density lipoprotein cholesterol and high levels of triglycerides. 32 In Italy, a sample of prepubertal children (3e11 years old), those with a WC above 90th percentile were more likely (19%) to have multiple risk factors (2), compared with children with values below the 90th percentile (9.4%). 33 Metabolic Syndrome: De Ferranti et al. 12 de?ned criteria for diagnosing MS in children and adolescents, similar to ATP-III criteria for adults. This de?nition seems well accepted now, and was recently quoted in a major publication that evaluated the various criteria in a population of 2624 teenagers, and was considered the criteria with the highest sensitivity, without losing speci?city. 34 Using these criteria in our cohort we identi?ed 8.8% of individuals with MS in 2006. The prevalence of MS in the population studied was consid- ered low. Studies of the Brazilian population have shown important changes in eating habits and physical activity. 35e40 We speculate about the negative in?uence on the historical longevity of this community because of the rates of MS, especially when associated with the cardiovascular risk parameters already discussed. The MS group had signi?cantly higher WC in 1999, indicating that WC has emerged nine years earlier than estimated in those children and adolescents that would evolve with MS. The BMI was also different, but did not reach statistical signi?cance. Waist circumference is an important element in screening patients for MS associated with other elements that lead to this diagnosis: triglycerides and LDL and HDL cholesterol, glucose and blood pressure. Many authors consider BMI as a better parameter to assess and monitor patients with MS 41,42 while others prefer WC. 3,4,31,32,43e45 Our study shows that the two parameters are good and that they correlate strongly with each other, but the WC has better expressed the evolution to MS. The population that participated in this analysis had distinctive ethnic characteristics, thus generalizing the results may be limited to white-caucasian populations of European origin, speci?cally of Italian origin. 5. Conclusions The?ndings of this analysis of the cohort of adolescents in Veranópolis indicate that waist circumference in children and adolescents is extremely useful in screening patients for metabolic syndrome and cardiovascular risk. WC is an anthropometric parameter of simple measurement, requiring less equipment costs, and this study was better than BMI, which had already been re- ported by other authors. 3,4,31,32,43e45 Fig. 2.Comparison of waist circumference (WC) in 2008 with visceral fat (VAT) and subcutaneous fat (SAT) in abdominal CT in 2008. [Pearson Correlation Coef?cient (r)]. Table 2 Comparison between waist circumference and body mass index in 1999 with diagnosis of metabolic syndrome in 2006. 2006 With Metabolic Syndrome Without Metabolic Syndrome p n¼14(8.8) n¼145(91.2) 1999 WC 80.9 13.2 71.9 10.3 0.03 BMI 23.9 5.1 21.2 3.7 0.07 Results presented in meanSD and categorical variablesn(%). WC¼waist circumference; BMI¼body mass index. Statistic: Studentttest for independent samples. J.V. Spolidoro et al. / Clinical Nutrition 32 (2013) 93e9796 As the WC in this population was associated with more subcu- taneous fat than visceral, it would be appropriate to evaluate the behavior of pro-in?ammatory cytokines and adiponectin to better understand the pathophysiology of these?ndings. Con?ict of interest The authors hereby declare that the article is original, is not under consideration for publication anywhere else and has not been previously published. Moreover, the authors declare no potential or actual personal, political or?nancial interest in the material, information or techniques described in the paper. Statement of authorship All authors state that all authors have made substantial contri- butions and?nal approval of the conceptions, drafting, and?nal version of the manuscript. Acknowledgments Manoel Pitrez was the coordinator of the trial. Luiz Vargas, João Santana, Eduardo Pitrez and Augusto Medeiros where responsible for the data collection. 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