Kaimbacher, Petra S.*; Dunitz-Scheer, Marguerite*; Wallner-Liebmann, Sandra J.†; Scheer, Peter J.Z.*; Sudi, Karl‡; Schnedl, Wolfgang J.§; Tafeit, Erwin||
The pattern of subcutaneous fat in children is of growing interest in the field of pediatric body composition. A better understanding of subcutaneous body fat distribution and body composition in children may influence the prognosis of adult health conditions and support the development of effective preventive strategies for reducing risk factors of diseases (1–3) such as obesity (2–8); metabolic syndrome (3,5–8); cardiovascular disease (3–8), including hyperinsulinemia (3,5–9); increased blood pressure; and atherogenic levels of blood lipids (4–8).
Various methods exist to evaluate body composition in children. Because of the necessary technical equipment, some of these methods are expensive, impractical, and inappropriate for use in field studies. The optical device LIPOMETER (EU Pat. No. 0516251) was developed to generate noninvasive, quick, accurate, and safe measurements of a monolayer of subcutaneous adipose tissue at any given site on the human body. Its technical features and validation results are based on computed tomography as a reference system and have been presented previously (10,11). The LIPOMETER allows the measurement of subcutaneous fat distribution and the determination of the so-called subcutaneous adipose tissue topography (12). Previous results (13–16) using the LIPOMETER to determine the subcutaneous adipose tissue topography emphasize the importance of describing subcutaneous adipose tissue in adult obesity and metabolic syndrome and during childhood and adolescence (17,18). A subcutaneous adipose tissue topography description of schoolchildren and children older than 7 years (17,18) has already been presented. Furthermore, a relation among subcutaneous adipose tissue layers, fat mass, and leptin in obese children and adolescents has been found (19,20).
The present study is the first to investigate and highlight subcutaneous adipose tissue topography in healthy infants (younger than 12 months) and children ages 1 to 7 years. The aim of the present study was to provide basic documentation of subcutaneous adipose tissue topography as a reference for characterizing deviations of subcutaneous adipose tissue in clinical samples. An accurate description of subcutaneous adipose tissue topography in healthy children may help describe various diseases, such as obesity, failure to thrive, and feeding and eating disorders, in relation to over- and malnutrition throughout childhood. In this basic documentation of subcutaneous adipose tissue topography, we focus on the description of healthy subjects during infancy and childhood analyzing the following:
1. The subcutaneous adipose tissue topography deviations in different age groups
2. The difference between female and male subcutaneous adipose tissue patterns for each age group
Previous findings for children older than 7 years (17,18) showed subcutaneous adipose tissue topography differences between different age groups. Because of these results, we investigated the hypothesis of subcutaneous adipose tissue topography differences between different age groups in our sample. In the previous studies (17,18), no sex differences in subcutaneous adipose tissue patterns in 7- to 11-year-olds were found. Sex differences started at age 11 years. Therefore, we anticipated as a second hypothesis no sex differences in the 0- to 7-year-olds.
SUBJECTS AND METHODS
The participants and their parents consented to the study after receiving a thorough explanation of the declaration of consent. The procedure chosen (EK-Nummer 20–415 ex 08/09) was in accordance with the Declaration of Helsinki and the local ethics committee's recommendations. Height or length, weight, upper arm circumference, waist circumference, and subcutaneous adipose tissue topography were measured in 275 children (147 boys and 128 girls) ranging in age from 0 to 7 years. The children were recruited in various schools, kindergartens, and infant day care centers from urban areas and in the local University Clinic for Pediatrics and Adolescent Medicine, where they consisted of visiting siblings and some patients in the aftercare phase.
This dataset was divided into 3 age groups (infant: 0–1 years, toddler: 1–5 years, child: 5–7 years) for each sex. The assignment of the 3 heterogeneous age groups in accordance with growth parameters was adapted from the definition of a standard pediatric textbook (21). The height of toddlers and children was measured using a stadiometer (SECA-220, SECA, Hamburg, Germany). The length of infants was measured using a standardized measurement device (SECA). Toddlers and children were weighed on a SECA scale (SECA-803), and infants were weighed on a RAUCH scale (RAUCH-WPT20D, Graz, Austria). The body mass index (BMI, kg/m2) was calculated. The description of the sample according to BMI percentiles is presented in Table 1(22,23). Furthermore, z score BMI values were calculated according to the Cole LMS method. This method adjusts the BMI distribution for skewness and expresses the BMI of individual subjects as an exact standard deviation (SD) score or z score (22–25). Upper arm and waist circumference were determined with an insertion tape (KAWE-REF E-43971, Kawe Kirchner & Wilhelm, Asperg, Germany). Upper arm circumference was determined using an inflexible tape on the nondominant arm from the midpoint between the acromion and the olecranon while the arm was stretched out. Waist circumference was taken from the midpoint between the iliac crest and the lower ribs measured at the sides.
Measurement of Subcutaneous Adipose Tissue Topography
The results of fitting LIPOMETER light patterns to absolute computed tomography values [N = 158] by regression analysis showed a correlation of r = 0.9863. There were no systematic deviations between the 2 methods (bias 0.00 ± 1.42) and small limits of agreement [−2.78 to 2.78] (10). To determine the subcutaneous adipose tissue thickness (in millimeters), the sensor head of the LIPOMETER is held at a perpendicular angle to the selected body site. Light-emitting diodes illuminate the subcutaneous adipose tissue layer, and the back-scattered light intensities are measured by a photodiode. These light patterns are converted into a subcutaneous adipose tissue thickness (10). To define the complete subcutaneous body fat distribution of a subject, 15 subcutaneous adipose tissue layers at specified body sites from neck to calf on the right side of the body are measured (17). For adults, the coefficients of variation of this set of 15 specified measurement body sites range from 1.9% (front chest) to 12.2% (rear thigh) (26). (For further details about the intraobserver reliability of adults, see previous publications (26,27)). In the present study, the intra- and interobserver reliability of children was provided in the 3 defined age groups for the first time (Table 2). The determination of the intra- and interobserver reliability is accompanied by a great deal of stress for the children because multiple measurements must be taken for each of the 15 defined measurement points; therefore 1 child per age group was selected. For the intraobserver reliability, the measurement of the 15 body sites was repeated 10 times and means and SDs were calculated. Finally, the coefficients of variation were calculated (coefficient of variation = SD/mean). For the interobserver reliability, the measurement of the 15 defined body sites also were performed 10 times. This set of 15 measurement points can describe a person's individual subcutaneous adipose tissue topography (12,28). Toddlers and children were measured in a standing position, whereas infants were measured while held on the lap of their primary caretaker. The determination of a person's subcutaneous adipose tissue topography takes approximately 2 minutes. The LIPOMETER is connected to a PC, which stores the data measured.
Some of the 15 measured body sites are situated in the same body region (eg, on the arms: triceps, biceps). Consequently, they exhibit similar fat development. To investigate the summed subcutaneous adipose tissue topography information of complete body regions (eg, arms, trunk), additional variables were calculated by summarizing the corresponding body sites:
Arms = biceps + triceps
Trunk = neck + upper back + lateral chest + front chest
Abdomen = upper abdomen + lower back + hip
Legs = front thigh + lateral thigh + rear thigh + inner thigh + calf
Total = arms + trunk + abdomen + legs
Notably, to provide information about the total amount of subcutaneous fat in healthy children, all 15 subcutaneous adipose tissue layers were summed (total subcutaneous adipose tissue).
Statistical calculations were performed by SPSS 16.0 for Windows (SPSS Inc, Chicago, IL). The hypothesis that the variables would be distributed normally was tested by the Kolmogorov-Smirnov test, in which a P value <0.05 was considered to be a significant deviation from normal distribution. Most of the 156 tested distributions (age, height, weight, upper arm circumference, waist circumference, 15 subcutaneous adipose tissue topography values, 4 subcutaneous adipose tissue topography body region values [arms, trunk, abdomen, legs], and total subcutaneous adipose tissue * 3 age groups * 2 sexes) were non-normal, and thus the median was calculated and the nonparametric Mann-Whitney U test for 2 independent samples was applied (28) for testing the differences between girls and boys and for testing differences between age groups (infant, toddler, child) for each sex. Additionally, topography plots were performed (17,28) to define the typical subcutaneous adipose tissue topography profile, showing the medians of the 15 subcutaneous adipose tissue layers for each sex and age group. Furthermore, stepwise discriminant analysis was used to investigate the discriminating power between female and male subcutaneous adipose tissue patterns in all age groups. Finally, a receiver operating characteristic (ROC) curve analysis was performed to calculate the power of our sample for the main research questions concerning the variation of fatness with time/sex. Therefore, the 2 groups that were used as input for the ROC curve analysis were infant and child. SPSS calculates an ROC curve for each of the 4 subcutaneous adipose tissue body regions (arms, trunk, abdomen, and legs) and the total subcutaneous adipose tissue, both of which are based on negative (age group infant) and positive (age group child) cases. Two different a priori hypotheses can be specified: that either smaller or larger parameter values are associated with stronger evidence of positivity (age group child). The area under the ROC curve is calculated. An area index of 0.5 provides a poor test (low discriminating power), whereas a value of 1.0 indicates an ideal test (high discriminating power). An area index <0.5 shows that the a priori hypothesis should be changed. Sensitivity and specificity were calculated for each of the 4 subcutaneous adipose tissue body regions (arms, trunk, abdomen, and legs) and the total subcutaneous adipose tissue. In the ROC curve, the x coordinate represents the sensitivity and the y coordinate shows the specificity. The highest sensitivity and specificity were obtained at the optimal cutoff point estimated by the Youden index (12,29,30). This optimal cutoff value provides the best discriminating power between the age group infant and the age group child, whereby smaller values are associated more strongly with the age group child.
Figure 1 presents the total subcutaneous adipose tissue distributions throughout the 3 defined age groups. Total subcutaneous adipose tissue in girls showed a highly significant decrease (P < 0.001) from the age group infant to the age group toddler and from the age group infant to the age group child (Tables 3 and 4). Between the age group toddler and the age group child, a significant decrease (P = 0.015) in total subcutaneous adipose tissue in girls was found (Table 3). Boys showed a highly significant decrease (P < 0.001) in total subcutaneous adipose tissue in all 3 age groups (Fig. 1, Tables 4 and 5). Girls showed a slightly lower relative reduction of total subcutaneous adipose tissue from infancy to childhood (−39.8%) than boys (−43.8%), but in absolute values, girls had a higher reduction in total subcutaneous adipose tissue (−45.2 mm) than boys (−42.7 mm). Girls also demonstrated significantly higher medians of total subcutaneous adipose tissue in the age group infant (P = 0.037) and the age group child (P = 0.008) (Tables 3 and 5, Fig. 1).
Figure 2 shows the decrease in subcutaneous adipose tissue in girls in more detail, whereby the 15 subcutaneous adipose tissue layers were summarized into 4 body regions: arms, trunk, abdomen, and legs. Arms did not significantly differ between the 3 age groups, whereas trunk, abdomen, and legs provided highly significant decreases (P < 0.001) of −42.7%, −30.2%, and −38.5%, respectively (Tables 3 and 4).
In boys, arms significantly (P = 0.035) decreased only from toddlerhood to childhood (−13.9%). The reduction of subcutaneous adipose tissue layers of trunk (−41.4%), abdomen (−50.2%), and legs (−46.7%) was highly significant (P < 0.001) between the age group infant and the age group child (Tables 4 and 5, Fig. 3).
In the various body regions, significant differences between girls and boys could be found in the age group infant and the age group child. Female infants showed significantly (P = 0.033) thicker subcutaneous adipose tissue layers of trunk than boys. In the age group child, girls had significantly higher subcutaneous adipose tissue layers of abdomen (P = 0.015) and legs (P = 0.010).
Figure 4 presents the topography plot of 128 girls divided into 3 age groups and shows the complete subcutaneous adipose tissue profiles. The highest absolute decrease from infancy to childhood (in millimeters) was that of rear thigh (−5.5 mm) with >50% difference from the starting point, followed by hip (−5.2 mm) and calf (−4.1 mm). The highest relative decrease was found in the neck (−62.1%). All 15 specified body sites, except triceps and lower back, significantly decreased from infancy to childhood (Table 3).
Figure 5 presents the topography plot of 147 boys divided into 3 age groups. The greatest decrease in millimeters was found in hip (−5.0 mm) with a −55.6% relative percentage. In boys especially, the trunk area (front chest −59.3%), the abdominal section (upper abdomen −50.0%, lower abdomen −54.2%), and the lower extremities (rear thigh −54.2%, calf −47.5%, front thigh −46%, inner thigh −44.3%) significantly differed. All 15 subcutaneous adipose tissue layers, except triceps, significantly decreased from infancy to childhood (Table 5).
Concerning the z score BMI in both sexes, no significant differences were found between the 3 defined age groups. The populations were the same in terms of adiposity within each age group (Tables 3 and 5).
In the age group infant, sex-specific differences could be found in the neck (P = 0.008), lateral chest (P = 0.012), hip (P = 0.041), lateral thigh (P = 0.016), and rear thigh (P = 0.044). In toddlers, sex-specific differences were lower: front chest (P = 0.041), lower abdomen (P = 0.035), and front thigh (P = 0.029). The strongest differences between female and male participants were found in the age group child. In particular, the trunk area with upper back (P = 0.016), front chest (P = 0.004), and lateral chest (P = 0.020); the abdominal section with upper abdomen (P = 0.018) and lower back (P = 0.003); and the legs with front thigh (P = 0.003), lateral thigh (P = 0.002), and inner thigh (P = 0.008) showing significantly sex-specific differences.
Finally, the discriminating power between female and male subcutaneous adipose tissue topography was investigated using stepwise discriminant analysis, which provided significant results for all 3 age groups. In the age group infant, a correct classification of 66.3% (P = 0.004) between subcutaneous adipose tissue topography of girls and boys could be made by stepwise discriminant analysis based on the significantly selected body site neck. In the age group toddler, 59.2% of original grouped cases could be classified correctly on the basis of lateral thigh (P = 0.048). In the age group child, the results of stepwise discriminant analysis showed that based on front thigh, lateral thigh, and rear thigh, a correct classification of 74.7% (P < 0.001) could be made.
In the present study, the exact subcutaneous adipose tissue topography description in healthy children ages 0 to 7 years is presented for the first time. The results of the subcutaneous adipose tissue measurements show a clear physiological decrease in subcutaneous body fat from infancy to childhood. The difference in the subcutaneous adipose tissue is presented on 3 levels: total subcutaneous adipose tissue, 4 body regions, and 15 body sites. The decrease (%) in subcutaneous adipose tissue from infancy to childhood was slightly higher in boys (−43.8%) than in girls (−39.4%), but in absolute values, girls show a minimally higher reduction in total subcutaneous adipose tissue (−45.2 mm) than boys (−42.7 mm). ROC curve analysis confirmed these main research results, namely the decrease in subcutaneous adipose tissue between infancy and childhood, and provided high discrimination power for our sample (Table 4). We received high area indices (up to 0.927) and high percentages of correctly classified cases (up to 90.1%) for the body regions trunk, abdomen, and legs and for the total subcutaneous adipose tissue of both sexes. For the body region arms, ROC results were not significant, which reconfirmed the Mann-Whitney U test (Tables 3 and 5).
Rolland-Cachera et al (31) correlated subscapular skinfold measured by caliper, with BMI providing the following results for infants (girls: r = 0.53–0.66, boys: r = 0.4–0.59), toddlers (girls: r = 0.44–0.56, boys: r = 0.43–0.57), and children (girls: r = 0.55–0.56, boys: r = 0.5–0.58). We tested total subcutaneous adipose tissue against BMI in 128 girls and 147 boys, finding higher correlations in all defined age groups with the exception of female infants. Our results showed correlations of r = 0.397 (P = 0.008) in female infants and r = 0.741 (P < 0.001) in male infants, r = 0.745 (P < 0.001) in female toddlers and r = 0.547 (P < 0.001) in male toddlers. In the age group child, we found a correlation of r = 0.763 (P < 0.001) in girls and a correlation of r = 0.889 (P < 0.001) in boys.
Concerning the interobserver reliability measured by caliper skinfolds, Heyward and Stolarczyk (32) stated coefficients of variation of triceps ∼3%, subscapular ∼3% to 5.0%, suprailiac ∼4%, abdomen 8.8%, and thigh 7.1%. Comparing these data to our results from the 3 age groups, we found coefficients of variation of triceps 6.7% to 7.6%, upper back (around the subscapular) 3.6% to 5.4%, hip (around the suprailiac) 7.9% to 9.4%, upper abdomen 5.4% to 6.7%, and front thigh 4.6% to 6.0% (Table 2). Coefficients of variation were higher at the body sites triceps and hip, equal on the body site upper back, and lower for upper abdomen and front thigh.
Subcutaneous fat accumulation represents the normal physiological buffer for excess energy intake (high-caloric diet). It acts as a metabolic sink where excess free fatty acids (FFAs) and glycerol are stored as triglycerides (TGs) in adipocytes (33). Therefore, the characterization of functional subcutaneous adipose tissue from childhood onward is important for further health and development.
It is well known that women in general store a larger amount of body mass as fat and are more likely to have subcutaneous fat on their lower extremities compared with men (34). This sex difference in adiposity is present at birth. Female infants have more subcutaneous fat than male infants for all gestational ages (35). In our study, girls also showed significantly higher total subcutaneous adipose tissue in infancy (P = 0.037) and childhood (P = 0.008) than boys. Girls showed significantly thicker subcutaneous adipose tissue layers in all 3 age groups in comparison with boys.
Stepwise discriminant analysis, which demonstrated significant results for all 3 age groups, also points to sex-specific subcutaneous adipose tissue pattern differences from infancy to childhood. In the age group infant, a correct classification of 66.3% between subcutaneous adipose tissue topography of girls and boys was made. In toddlers, the sex-specific differences were lower (59.2% correct classification). The strongest differences between female and male subjects (74.7% correct classification) were found in the age group child (5–7 years), which was caused by a stronger decrease in abdomen and legs in boys (Figs. 2 and 3). Previous results (17) found no significant differences between 7- to 9-year-old girls and boys, but sex-specific differences in the subcutaneous adipose tissue topography development were found during prepuberty and adolescence.
Another issue is the fact that women use more nutrients during reproduction. In females, fat and fertility are linked through leptin. Low leptin levels reduce fertility (34,36,37). The ovarian function of adult women is associated with their adipose mass at birth. Throughout human evolution, food scarcity has been a frequent occurrence. Women have benefited from a more efficient ability to store fat (34). The subcutaneous fat depot is the major source of leptin, a hormone also strongly involved in fat mass stability and satiety (38). Approximately 80% of all body fat is subcutaneous (38,39). The results of the present study support these facts and the importance of monitoring subcutaneous adipose tissue from childhood onward.
One interesting finding was that the decrease in body fat distribution happens mainly in the trunk, abdomen, and lower extremities, whereas the body fat distribution of the upper extremities did not significantly differ between the 3 defined age groups.
Small adipocytes, found in great number in subcutaneous adipose tissue, are more insulin sensitive and have high avidity for uptake by FFAs and TGs, preventing their deposition in nonadipose tissue (40,41). Subcutaneous adipose tissue in the abdominal wall has shown the highest rate of uptake of TGs and larger FFA release per kilogram (40,42). Further studies are necessary to investigate the origin and meaning of these initial results.
The present study was a cross-sectional study and does not provide longitudinal data for anthropometric data for each child. Presently, neither studies assessing longitudinal changes in body fat distribution nor comparable cross-sectional studies in children ages 0 to 7 years exist.
Our study was the first to our knowledge to be able to generate basic documentation of subcutaneous adipose tissue topography during infancy and childhood in healthy children. In the near future, this documentation may contribute to further scientific research for characterizing deviations of subcutaneous adipose tissue topography in clinical samples.
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