Introduction

The prevalence of obesity in children has increased dramatically over the last 20–30 y. In 1988–1991, the prevalence of all children with BMI greater than the 95th percentile was 11%, while 22% were above the 85th percentile.¹ Even more disturbing is the fact that the prevalence of overweight and obesity increased more dramatically in some ethnic groups, such as African American children. Though in most cases, African American children had a lower prevalence of overweight and obesity than white children in the 1963–1970 time period, the most recent surveys demonstrate higher rates of overweight and obesity among African American children, as compared to white American children. Given this rapidly increasing prevalence of obesity in African American children, and the high rate of obesity in African American adults,² it is important to identify factors related to these trends.

The prevalence of pediatric type 2 diabetes has increased rapidly over the last 20 y. For example, the incidence of type 2 diabetes in adolescents was estimated to increase ten-fold from 1982–1994 in the greater Cincinnati area.³ Sixty-eight percent of the adolescents presenting with type 2 diabetes were African American, while only 14.5% of the population served by this medical center were African American. This confirms the disproportionate presentation of diabetes in some ethnic groups, such as African American people.⁴ The high relative weight of these children (mean age 13.8 y, mean BMI 37.7 kg/m²), along with the known association between obesity and type 2 diabetes, suggest that this rapid rise in type 2 diabetes among adolescents is related to the rapid rise in obesity.

Ethnic differences in the risk factors potentially related to obesity and type 2 diabetes are also being identified, and may be indicative of different etiologies or thresholds of effect. It has been noted, for example, that African American individuals tend to have higher insulin levels, and greater insulin resistance than white individuals.^5,6,7,8,9,10 As it is known that visceral abdominal fat is associated with insulin resistance, it was postulated that this ethnic difference in insulin level and insulin resistance may be related to differences in body composition. Though the data do suggest that visceral abdominal fat is associated with insulin resistance in African American individuals,^11,12,13,14 the studies also show that African American have relatively less visceral abdominal fat than white individuals.^11,13 Given the higher level of insulin resistance among African American individuals, this is the opposite of what would be expected. This experience and others related to this issue suggest that the associations between obesity, regional fat, and type 2 diabetes among the African American population are complex and require more investigation.

Given the peak incidence of pediatric type 2 diabetes in adolescence,³ and the known increase in insulin resistance which occurs during adolescence,⁴ evaluating these factors in children and adolescents is important and appropriate. However, limited information is available regarding these factors in children and adolescents, especially obese children and adolescents. Thus this study was undertaken to evaluate body composition, including visceral abdominal fat, and the metabolic factors, insulin, glucose, and leptin levels, and the homeostasis model assessment of insulin sensitivity (HOMA-IR),¹⁵ in obese African American and white children and adolescents.

Methods

Subjects

6–18-y-old obese children and adolescents entering The Children's Hospital of Philadelphia Weight Management Program were considered for participation in the study. To be eligible children had to be greater than 150% of ideal body weight, and to not have another condition which impacts on body composition, hyperlipidemia, or insulin/glucose homeostasis. Participants were evaluated prior to initiating weight loss or significant lifestyle changes. A parent or guardian of each participating child consented to participation. The protocol was approved by the Children's Hospital Institutional Review Board. Subjects were instructed to fast for 12 h prior to the initiation of the studies. Studies were completed in the General Clinical Research Center at The Children's Hospital of Philadelphia.

Anthropometric and other measurements

Height was measured using a wall-mounted stadiometer. Weight was measured with an electronic scale. Standard anthropometric methods were utilized.¹⁶ Measurements were completed twice and average values utilized in the analyses. Each participant's Tanner stage was determined by a physician in the Weight Management Clinic.^17,18

Body composition

A single midline sagittal CT scan (Siemens Somatom Plus 4, Siemens, Iselin, NJ) was used to locate L4. To assess abdominal fat, a single 10 mm thick CT scan at L4 was completed. The cross-sectional fat area of each scan was assessed by quantifying the area of each scan with a density between -250 and -50 Houndsfield units.¹⁹ The total fat area (referred to as total CT fat), visceral abdominal fat (referred to as visceral CT fat), and subcutaneous abdominal fat (referred to as subcutaneous CT fat) were assessed for each scan.

Body composition was assessed by DEXA using a Hologic QDR2000 instrument (Hologic, Waltham, MA). Subjects were scanned in fan beam mode and analysed using the Enhanced Whole Body V5.71A software provided by Hologic. The information derived from the scan includes bone mass, fat mass (total body), lean body mass, and fat free mass (lean body mass plus bone mass).

Laboratory Analyses

Blood samples were drawn in the morning after the subject had fasted for 12 h. Serum samples were analysed for insulin and leptin level in the Children's Hospital General Clinical Research Core Laboratory, while glucose was assessed in the Children's Hospital Clinical Chemistry Laboratory. Glucose measurements were made on a Vitros 950 Chemistry Analyzer (Ortho Clinical Diagnostics, Raritan, NJ) using a glucose oxidase method. Insulin (ALPCO) and leptin levels (Diagnostic System Laboratories) were analysed by ELISA.

Statistical analysis

Age, gender and race specific BMI Z-scores were derived from the BMI reference standards developed by Rosner et al.²⁰ Insulin resistance was estimated using the homeostasis model assessment of insulin sensitivity (HOMA IR),¹⁵ which has been shown to mirror the glucose clamp technique in the assessment of insulin sensitivity,²¹ and also strongly predicts the development of diabetes in at-risk populations.²² HOMA IR was calculated using the formula: HOMA IR=insulin (U/ml)  Glucose (mmol/l)/22.5. A higher HOMA-IR score suggests a greater degree of insulin resistance.

Data were compared for the African American and white children and for the boys and girls. The group means of the body composition and metabolic variables were compared by t-test and Mann–Whitney U-test, as appropriate. The influence of potential covariates (eg age, pubertal status) was assessed using analysis of covariance. The associations between the body composition and metabolic variables were assessed using Pearson and Spearman correlations. The significant associations were subsequently re-examined with potential covariates included in the analyses. Log transformations were utilized to adjust for skewed distributions, as appropriate. Thirty-six children were assessed. It was determined that five children had not fasted as instructed; thus results for insulin, glucose, HOMA IR, and leptin levels for these children were not included in the analyses. Analyses of ethnic group differences were limited to the African American and white children only. Statistical significance was defined as P<0.05. SPSS for Windows (version 7.0, SPSS, Inc, Chicago, IL) was utilized for the analyses.

Results

The characteristics of all the participants together, and for the boys, girls, African American, and white children are listed in Table 1. The groups did not differ significantly on age, BMI Z-score, Tanner stage, fat-free mass, % body fat, or visceral CT fat. The boys had a higher mean glucose level compared to the girls (P=0.02). This was still significant after adjusting for age or pubertal status. Compared to the white children, the African American children had a higher BMI (P=0.05), fat mass (P=0.03), total CT fat (P=0.04), subcutaneous CT fat (P=0.03), insulin level (P=0.003), leptin level (P=0.02), and higher HOMA IR (P=0.007). However, these differences were not significant after adjusting for age or pubertal status. In addition, the ethnic group differences in total abdominal fat and subcutaneous abdominal fat were not significant after adjusting for total body fat or BMI. Previous publications have described lower visceral abdominal fat for African American people. Since the African American children in our study had greater body fat, it was postulated that a true ethnic difference in visceral CT fat was obscured by the greater overall body fat. However, after adjusting for total body fat, still no ethnic group difference in visceral CT fat existed.

Table 1 - Characteristics of obese children and adolescents.

Full table (35K)

Regarding the metabolic factors, the ethnic group difference in leptin level was not significant after adjusting for total body fat, or subcutaneous CT fat. However, the ethnic difference in insulin level remained after adjusting for total body fat (P=0.03), and subcutaneous CT fat (P=0.01). Similarly, the ethnic group difference in HOMA IR remained after adjusting for total body fat (P=0.05), and subcutaneous CT fat (P=0.03).

The correlations between the metabolic factors and the measures of body composition or relative weight were assessed (Table 2). Insulin and HOMA IR were significantly associated with fat mass and leptin level. The association between leptin and insulin levels, and between leptin and HOMA IR, were still significant after controlling for total body fat. Leptin levels correlated significantly with fat mass, fat free mass, total CT fat, and subcutaneous CT fat. The associations between leptin and total CT fat and subcutaneous CT fat were not significant after controlling for total body fat. However, the significant association between leptin and fat free mass remained after adjusting for total body fat (P=0.04). None of the metabolic variables were significantly associated with visceral abdominal fat.

Table 2 - Correlation between metabolic factors and body composition.

Full table (20K)

Discussion

This assessment of the body composition and regional fat distribution of obese children and adolescents failed to identify gender or ethnic group differences (between African American and white children) in regional fat distribution, independent of total body fat, age or pubertal status. Evaluation of the association between the metabolic factors, insulin, and insulin resistance (as measured by HOMA IR), and leptin levels also demonstrated that these factors were associated with total body fat, but not regional fat distribution (eg visceral abdominal fat or subcutaneous fat). As described below, these results differ somewhat from results previously reported for adults and non-obese children.

Obesity is associated with altered insulin/glucose homeostasis. Investigation of body fat distribution has shown that visceral abdominal fat is strongly associated with insulin resistance, and other factors.^{14,23,24,25,26,27,28} However, in the results reported now, visceral abdominal fat was not correlated with insulin level or HOMA IR for the obese children and adolescents. Recent new information also suggests that subcutaneous fat may be associated with insulin resistance, especially in African American people. For example, Lovejoy et al²⁹ showed subcutaneous abdominal fat was associated with fasting insulin level and insulin sensitivity in young African American women, but not young white women. Yanovski et al³⁰ reported similar findings relating to normal weight 7–10-y-old girls. Our study did not confirm this relationship between subcutaneous fat and insulin resistance. However, the observed relationship between insulin level and total body fat in our study is consistent with findings reported by Gower et al.¹⁰ The inconsistencies in these observations between studies could be related to the reported differences in body composition-metabolic factor associations between obese and non-obese individuals,²⁴ and suggest the complexity of these relationships. In addition, in our study, visceral fat levels were a relatively small proportion of abdominal fat and total body fat of the children studied. It could be postulated that the effect of the visceral fat is overshadowed by the effect of total body fat in these obese children. The relatively higher amount of visceral abdominal fat of adults may make it more important physiologically in adults, as compared to children. Further evaluation of these ethnic and life cycle factors in obese and non-obese subjects is needed to clarify these relationships.

Insulin sensitivity and insulin response are major components of the pathophysiology related to obesity and type 2 diabetes. Higher fasting and 2 h (post-oral glucose) insulin levels have been described in the African American adults, as compared to white adults.^5,31,32 These findings are independent of regional fat distribution. Such ethnic differences relating to glucose/insulin homeostasis seem to be consistent across a broad age range and in obese and non-obese individuals. For example, African American children (7–11-y-old) have higher insulin levels than white children, independent of total body fatness.⁹ Schuster et al³² evaluated white and African American lean and obese adolescents; within racial groups, the obese adolescents had an increased insulin response during the oral and intravenous glucose tolerance tests. Obesity also seemed to have a greater effect on insulin resistance in African American adolescents than white adolescents; comparing the obese adolescents, obese African Americans had increased baseline insulin levels and insulin response when compared to obese white adolescents. Arslanian reported similar findings regarding the insulin response, but did not note an ethnic difference in baseline insulin level in healthy adolescents.⁷ Data from the Bogalusa Heart Study⁶ describe higher insulin levels among African American adolescents (compared to white adolescents). Our results, when compared with those published for non-obese individuals,²¹ do suggest a difference in insulin resistance between obese and lean children. However, we did not identify an ethnic difference in insulin resistance independent of age or pubertal status. This raises the possibility that ethnic group differences in insulin resistance differ in obese and non-obese children. Further evaluation of functional tests of glucose control among obese children would be informative.

Leptin is secreted by adipose tissue.³³ Leptin levels have been shown to be associated with fat mass and dietary intake/energy balance. Leptin is thought to act as a signal of the level of adiposity, to the mechanisms that control dietary intake, and possibly of energy expenditure.^34,35,36 Leptin levels are also associated with insulin levels,^8,34 but not insulin sensitivity. Higher leptin levels were reported in African American girls, which may be expected given the higher insulin levels observed in African American people.³⁴ However, other studies have not reported ethnic differences in leptin levels.^37,38 At the other extreme, lower leptin levels were reported in obese, post-menopausal African American women.³⁹ In our study, the ethnic group differences in leptin levels was not independent of total body fat, age, or pubertal status. However, leptin levels were associated with insulin levels and HOMA IR, independent of total body fat and subcutaneous abdominal fat. This suggests that children and adolescents with greater insulin resistance may have higher leptin levels. This could be consistent with leptin resistance in those with high insulin levels, or an adaptive mechanism to help prevent further weight gain (through leptin's influence on body weight).

The association between the leptin level and fat free mass is more difficult to explain. Fat mass and fat free mass are significantly correlated; however, fat free mass and leptin level were still significantly associated even after adjusting for fat mass. Recent information has described a correlation between insulin resistance and intramuscular fat.^40,41 However, intramuscular fat makes up only approximately 3% of thigh adipose tissue. It seems doubtful that the potential error in DEXA fat-free-mass estimation caused by this small amount of intramuscular fat would account for the positive relationship between total body fat free mass and insulin level or leptin level. These results require further evaluation.

One disturbing finding of the study is the degree of insulin resistance observed in these obese children. Sixty-nine percent of the participants had elevated insulin levels (>20 mcU/ml). Assessing the HOMA IR results is somewhat more difficult due to limited comparison data. Kawabe et al⁴³ reported a mean (s.d.) HOMA IR of 1.70.5 for 17–18-y-old boys who did not exercise regularly (n=114, BMI= 20.72.6). Similarly, a study of measures of insulin resistance reported HOMA IR<1.6 for non-diabetic adult males.¹⁵ Despite the limited information, the mean HOMA IR of 4.8 for these obese children and adolescents suggests an important degree of insulin resistance, and further suggests that obese children and adolescents should be tested for insulin resistance.

Our study does have certain limitations. The small sample size limits the power of the analyses. However, the similarities between our findings and those previously published support the validity of our findings. Furthermore, no functional measure of insulin response and insulin resistance was available. Though HOMA IR has been shown to be a relatively accurate measure of insulin resistance,²¹ utilizing a functional test of insulin response, along with a large sample size should be considered for future studies of these ethnic and gender differences.

Thus, this study of body composition, regional fat distribution and metabolic factors of obese children and adolescents, underscores the complexity of these relationships in an ethnically diverse sample, and presents some novel findings not seen in previous studies. Given the epidemic of pediatric obesity and type 2 diabetes,³ and the limited data relating to children, and especially obese children, it is essential to gain a better understanding of the factors, such as body composition and insulin resistance, associated with this epidemic.

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Acknowledgements

This project was sponsored by The Children's Hospital of Philadelphia General Clinical Research Center (MO1RR00240). These results were partially presented at the 2001 Pediatric Academic Societies Annual Meeting.