Objective: As skinfolds from four-sites (triceps, biceps, subscapular, suprailiac) and body fat percentage in 6-17 years is lacking in Turkey. This study was undertaken to produce references for four-site skinfolds and body fat percentage in children and adolescents.
Methods: The cross-sectional study was conducted between September 2007-May 2008 in Kayseri, Turkey, after approval by ethics committee of Erciyes University and local educational authority. Data were obtained from the Determination of Anthropometric Measures of Turkish Children and Adolescents Study-II. Using multistage sampling method, 4285 children were selected from the schools representing city centre, rural and urban areas of the province. Skinfolds were measured from four sites and body fat percentage was calculated according to Westrate and Deurenberg equation. LMS Chart Maker Pro version 2.3 software was used to obtain skinfold references.
Results: There were 1914(44.6%) boys, 2371(55.3%) girls in the study; the age range being6-17 years. The peripheral skinfolds increased with age for girls (7.2 mm at age 10 versus 8.7 mm at age 17), while this was true for boys until 10 years (6.2 mm at age 10 versus 4.2 mm at age 17) after which the values gradually decreased. In terms of central skinfolds, girls had higher numbers in each age (11.7 mm for boys versus 12.8 mm for girls at age 6; 24.9 mm versus 26.3 mm at age 17).
Conclusion: Skinfolds and body fat percentage provide information that helps monitor secular trends in obesity in Turkey and may be used to make national and international comparisons in the future.
Keywords: Anthropometry, Body fat percentage, Obesity, Skinfolds, Turkish children. (JPMA 64: 1154; 2014).
The assessment of body composition is an important issue of current paediatric research to investigate the effect of lifestyle interventions on body compartments as fat and fat-free tissues.1
Body mass index (BMI) is often used as a surrogate marker, but it does not provide an accurate assessment of body fat.1 More sensitive and accurate methods for assessing body composition like underwater weighing, plethysmography, magnetic resonance imaging (MRI) and dual-energy X-ray absorptiometry (DEXA) are difficult to be accessed for daily clinical practice and epidemiologic studies.2 Thus, skinfolds can be considered a "midway" marker that is more sensitive than BMI in determining body fat and is more useful for both clinical applications and epidemiological studies than the more sensitive methods.3,4 Additionally, skinfold thickness determines nutritional status and assesses disorders and/or diseases related to malnutrition and obesity.
Different body regions where skinfold thickness is measured may indicate different patterns of fat distribution. Triceps and biceps skinfolds reflect peripheral fat, whereas subscapular and suprailiac skinfolds refer to central/visceral fat. The present study was planned to provide references for triceps, biceps (peripheral fat) and subscapular and suprailiac (central fat) skinfold thicknesses and also body fat percentages derived from these four indices in Turkish children and adolescents.
Subjects and Methods
The cross-sectional study was conducted between September 2007 and May 2008 in Turkey\'s Kayseri province. Data was obtained from the study of the Determination of Anthropometric Measures of Turkish Children and Adolescents (DAMTCA II)5 which was performed in the same region that has more than 1,200,000 inhabitants and is a leading industrial trade center in Turkey. The study protocol was approved by the Ethics Committee of Erciyes University and the administration of the local educational authority.
Using multi-stage probability sampling for school children living in Kayseri, 4285 subjects were recruited for the study from 17 randomly selected schools including (primary, secondary and high schools) from both public and private sectors. Once the schools were selected, the students were recruited according to their ages. Children with known growth disorders and those taking any kind of medication were excluded. Chronological age was calculated as the decimal age by substracting the observation date from the birth date. Each year elapsed from their birthdates was noted as one age (e.g. 6.00-6.99 is accepted as six years of age). Parents\' written consent was obtained prior to the study, and the procedures were in accordance with those outlined by the Declaration of Helsinki.
Each of the four sites of measurement (triceps, biceps, subscapular, suprailiac) was marked carefully before measurement. All marks and measurements were made on the left side of the body. The procedure was explained to the child before taking the measurements. All measurements were taken using Holtain skinfold calipers. The skinfold thickness was measured to the nearest 0.1mm, while the fingers continued to hold the skinfold. The actual measurement was read from the caliper about 3 seconds after the caliper tension was released.6
For peripheral skinfolds, triceps was measured at a marked midpoint in the posterior surface of the left upper arm between the acromium and the olecranon process, at the point previously marked for the mid-upper-arm circumference. The child stood upright with weight evenly distributed and feet together, shoulders relaxed, and the arms hanging freely at the sides. The biceps was measured at the same point, but in the anterior line of the arm.6
For central skinfolds, subscapular was measured with the child standing erect with shoulders relaxed and arms hanging loosely at the side. The inferior angle (or triangle portion) of the left scapula was palpated and a cross (+) was made on the inferior angle of the scapula. The suprailiac was measured by lifting a horizontal skinfold at the suprailiac area, about 2cm above the iliac bone.6
Due to the large sample size, pubertal stages were not determined, thus body fat percentage was calculated with Westrate and Deurenberg equation.7
For statistical analysis, construction of the centile curves was performed with LMS Chart Maker Pro version 2.3 software (The Institute of Child Health, London), which fits smooth centile curves to reference data. This method summarises percentiles at each age based on the power of age-specific Box-Cox power transformations that are used to normalise data. The final curves of percentiles are produced by three smooth curves representing L (Lambda; skewness), M(Mu; median), and S (Sigma; coefficient of variation). These three quantities depend on age.8
The 17 schools in the study represented 2.4% of the 708 schools in the region. Of the 4285 subjects, there were 1914(44.6%) boys and 2371(55.3%) girls; the overall age range being 6-17 years. Smoothed and weighed age- and gender-specific LMS values for peripheral (triceps and biceps) and central (subscapular and suprailiac) skinfold thicknesses and the sum of skinfolds and body fat percentages were calculated (Table-1A, 1B).
The peripheral skinfolds increased with age for girls (7.2mm at age 10 versus 8.7mm at age 17), while this was true for boys until 10 years (6.2mm at age 10versus 4.2mm at age 17 for boys) after which the values gradually decreased (Table-2).
In terms of central skinfolds, girls had higher numbers in each age group (11.7mm for boys versus 12.8mm for girls at age 6; 24.9mm versus 26.3mm at age 17) (Table-3).
For both boys and girls, the sum of skinfolds increased with age and girls had higher sum of skinfolds than boys at each stage (17mm for boys and 18.3mm for girls at age 6 versus 20mm and 31.8mm at age 17). The body fat percentage increased with age for girls (11.3% at age 6 versus 13.8% at age 17), while this was true for boys until 10 years after which the values gradually decreased (10% at age 10 versus 9.2% at age 17). In each age, girls had higher body fat percentage than boys (Table-4).
In both genders, the sum of skinfolds gradually increased between 6 and 17 years, but decreased in peripheral skinfolds for the boys (Figures-1-3).
Although BMI is the primary measure to assess overweight and obesity, but it is difficult to discriminate between fat and fat-free mass and also the distribution of fat content in different body compartments. Smoothed percentiles of skinfold thicknesses from different sites will allow better assessment of fat and fat-free mass and also the distribution of fat content.9 The primary contribution of this study is to provide references — both skinfold references (triceps, biceps, subscapular, suprailiac) and body fat percentages (calculated by Westrate-Deurenberg equation).
Triceps skinfold is the main reference for total body fat reserves and the marker is sensitive to changes in the nutritional status of both children and adolescents.10-12 Triceps skinfolds have been used to determine total body fat percentage in Spanish boys and adolescents.13
As it is relatively easy and more common to measure triceps skinfolds, the current literature has several studies providing the mean values from different countries.14-18 However, in most of these studies, age distribution is found lacking.14-16,18
In two studies,19,20 data was used to perform comparisons. In boys, smoothed triceps skinfolds were higher than the two studies — one each in the US and Germany — for 3rd and 50th percentiles. For 97th percentile, the values were similar around 11 years with US boys; afterwards US boys had higher values than their Turkish counterparts. German boys had lower values than those of US and Turkey. In girls, triceps skinfolds were higher than US and Germany for 3rd percentile. For the 50th percentile, the values were similar around 13.5 years, while US had higher values afterwards. Germany had lower values than US and Turkey. For the 97th percentile, Turkey and US had similar values until 9.5 years. Afterwards, US had higher values. German girls had lower values than US and Turkey.
Two other studies are also relevant; one in Nepal21 (6-10 years) and the other on Pakistani children living in Bahrain22 (5-17 years)Among boys, Turkey had higher mean values than Pakistan until 9.5 years, after which Pakistan had higher values, while Nepal had the lowest. Among the girls, Turkey had slightly higher values than Pakistan until 10 years; but afterwards Pakistan had higher values, while Nepal had the lowest.
In our previously published data comprising 5553 Turkish children and adolescents aged 6-17 years, triceps skinfolds increased with age for girls, while this was true for boys until 11 years, after which the values gradually decreased.23 Similar results were obtained in the current study with only one exception for boys: the increment in triceps was until 10 years.
Triceps skinfold reflects the relative distribution of fat in the subcutaneous compartment. There is a major disadvantage of using it alone in children and adolescents. However, mean normal values for tricep skinfolds differ with age and gender, and values for children and adolescents of different ages cannot be compared without reference to age-related norms. It is recommended to use triceps skinfolds that can be expressed as a percentile distribution, the standard deviation score or percentage of mean value for age is used. Thus, the percentile distribution of triceps and additional three sites (biceps, subscapula, suprailiac) were provided in the present study.
Regarding biceps, in boys, Turkey had higher mean values than Pakistan22 until 11.5 years, followed by a gradual decrease. Pakistan had the highest values for 12 and 14.5 years. In girls, Turkey had higher values than Pakistan for 11.5 years, the values gradually decreased, and Pakistan had the highest values for 15.5 years, and a decrease was seen afterwards.
Although triceps and biceps are primary references for total body fat and are sensitive to the changes in nutritional status of both children and adolescents,10-12 they also reflect the relative distribution of body fat. The most prominent finding was similarity of triceps and biceps references between each gender and significant difference thereafter until 17 years. This finding is consistent with the results of another study.24 This prominent difference was considered a result of significant decrease in both triceps and biceps references in boys. This change in peripheral fat can be explained by the compartmental shift from fat to fat-free mass in boys. On the other hand, in both genders, central skinfolds, subscapular and suprailiac, both increased from 6-to-17 years in children and adolescents. The similarity in central fat accumulation indices, but decrease in peripheral fat indices for boys may be explained by male type body formation during pubertal period. We can conclude that peripheral fat accumulation is more sensitive than central in response to pubertal development.
In terms of central skinfolds, subscapular were compared to the four studies cited above.19-22
In Turkish boys, subscapular skinfolds were higher than US and Germany for 3rd and 50th percentiles. For the 97th percentile, Turkey and US matched each other around 10.5 years and US values exceeded Turkey beyond that point. In girls, subscapular skinfolds were higher than US and Germany for 3rd and 50th percentile. For the 97th percentile, Turkey had higher values than US around 8.5 years, but US exceeded Turkey after that. Germany had the lowest values for both genders for subscapular skinfolds.
Besides, Turkish boys had higher mean subscapular skinfolds than Pakistani boys until 10 years, after which they had higher values. The highest mean skinfolds were seen around 14.5 years for boys and girls, while Nepal had the lowest values for both genders.
For suprailiac skinfolds, comparisons were performed with the Pakistani study.22 Turkish boys had lower suprailiac skinfolds than Pakistani boys for 6 years, but after 7 years, Turkey had higher values until 11.5 years. Pakistan had higher values afterwards and two great increases were observed around 12 and 14.5 years. There were sharp decreases in 13 and 16 years. Turkish girls had lower suprailiac skinfolds than Pakistani girls for 6 years, but after 7 years Turkey had higher values until 10.5 years. After 11.5 years, Turkey had lower values than Pakistan until 12.5 years, and the values gradually increased until 14 years for Turkey, while Pakistan had higher values beginning from 11.5 years. Pakistan skinfolds decreased at 15.5 years, getting lower than Turkey, but increased afterwards.
In the current study, the sum of four skinfolds were computed and body fat percentage was calculated according to Westrate and Deurenberg equation.7 Body fat percentage is an evidence for risk of obesity for children and adolescents. The median (50th percentile) body fat percentage values for Turkish boys increased from 16.8% (at age 6) to 17.5% (at age 10). At age 11, the values began to decrease from 17.0% to 15.2% (at age 17). The median values for Turkish girls gradually increased from 26.9% (at age 6) to 53.8% (at age 17).
Countries like Germany19 and US20 have skinfold LMS values for age, but none of them computed the Westrate and Deurenberg equation to calculate body fat percentage. There is only one study from Italy (mean age: 15.4 years) which used the same equation,15 and according to its results, the body fat percentage for Italian boys and girls were 19.3±5.6 and 23.3±4.4%, respectively. In the current study, Turkish boys had lower body fat percentage than their Italian counterparts at each age (with having the highest value as 17.7% at age 9). Turkish girls had lower body fat percentage than their Italian counterparts at each age (with having the highest value as 20.0% at ages 16 and 17). This may indicate a lower trend towards obesity in Turkish children and adolescents, and they tended to have a lower risk of obesity than their Italian counterparts.
In general, global researches have tended to calculate body fat percentage by using Slaughter equation (including triceps and subscapular skinfolds)25,26 or Yuan equation27 rather than measuring four sites and computing other equations to predict body fat percentage. Besides, some others have preferred to use sum of skinfolds, without calculating body fat percentage.28-30
When using the Slaughter equation, the pubertal stage should be determined. A study from the United Arab Emirates (UAE) calculated body fat percentage with another pubertal stage-requiring method called the Deurenberg equation (including four sites).31 Even though it seems more practical to measure two sites, it is not always easy to assess pubertal development. Due to our study\'s nature (a cross-sectional one with 4285 children) and the difficulty of employing a paediatrician for every school and socio-cultural differences, we did not determine pubertal stages.
From a general point of view, body fat percentage of Turkish boys was higher for ages 6-to-11, 13, 15-to-17, while Turkish girls were higher for ages 6-to-12, than the other countries.
The results of the present study indicate that the skinfolds measured from four sites for Turkish children and adolescents were similar mostly to their Pakistani counterparts. Girls exerted significantly higher percentiles for skinfolds from four sites than boys in each age. In general, the body fat composition of Turkish children and adolescents in the current study reflected peripheral (subcutaneous) rather than central (visceral) fat deposition. Further multi-site, nationwide, prospective, longitudinal studies will provide much more reliable data to produce new references in the future.
So far, this is the most comprehensive study based on a representative sample of Turkish children and adolescents indicating precise evaluation of body fat percentage using skinfold thickness from four sites. The early detection of abdominal fat stores using our data and respective body fat percentage may now be implemented in routine clinical practice. As we provided sufficient number of percentiles (3rd to 97th) for four sites, sum of four sites, and body fat percentage, therefore our data may be a good reference for the evaluation of overweight and obesity status. In order to evaluate the body fat status of children, four-site results may be a beneficial reference. In the light of our results, the change in four sites within ages may be monitored to assess the overweight and obesity status among children for both national and international comparisons.
We are grateful to the principals, teachers, students and parents for their participation and cooperation, and to Volkan Ozkaya (MSc; Dietician) for his kind assistance.
1. Kriemler S, Puder J, Zahner L, Roth R, Meyer U, Bedogni G. Estimation of percentage body fat in 6- to 13-year-old children by skinfold thickness, body mass index and waist circumference. Br J Nutr 2010; 104: 1565-72.
2. Silva DAS, Pelegrini A, de Lima e Silva JMF, Petroski EL. Epidemiology of whole body, peripheral and central adiposity in adolescents from a Brazilian state capital. Eur J Pediatr 2011; 170: 1541-50.
3. Olds T, Tomkinson G, Dollman J. Secular trends in the skinfold thicknesses of young people in developed countries. J Hum Ecol 2007; 15: 41-49.
4. Durnin JV, Rahaman MM. The assessment of the amount of fat in the human body from measurements of skinfold thickness. Br J Nutr 1967; 21: 681-9.
5. Mazicioglu MM, Kurtoglu S, Ozturk A, Hatipoglu N, Cicek B, Ustunbas HB. Percentiles and mean values for neck circumference in Turkish children aged 6-18 years. Acta Paediatrica 2010; 99: 1847-53.
6. Harrison GG, Buskirk ER, Carter JEL, Johnston EF, Francis E, Lohman TG, et al. Skinfold thickness and measurement technique. In: Lohman T, Roche AF, Martorell R, (eds.) Anthropometric Standardization Reference Manual. Champaign, IL: Human Kinetics Book, 1988.
7. Westrate JA, Deurenberg P. Body composition in children: proposal for a method for calculating body fat percentage from total body density or skinfold-thickness measurements. Am J Clin Nutr 1989; 50: 1104-15.
8. Cole TJ, Green PJ. Smoothing reference centile curves: The LMS method and penalized likelihood. Stat Med 1992; 11: 1305-19.
9. Geiss HC, Parhofer KG, Schwandt P. Parameters of childhood obesity and their relationship to cardiovascular risk factors in healthy prepubescent children. Int J Obes Relat Metab Disord 2001; 25: 830-7.
10. Mascarenhas M, Zemel B, Stallings V. Nutritional assessment in pediatrics.Nutrition 1998; 14: 105-15.
11. Rolland-Cachera M. Body composition during adolescence, methods, limitations and determinants. Horm Res 1993; 39: 25-40.
12. Sardinha LB, Going SB, Teixeira P, Lohman T. Receiver operating characteristics analysis of body mass index TST and MAC for obesity screening in children and adolescents. Am J Clin Nutr 1999; 70: 1090-5.
13. Sarria A, Moreno LA, Garcia-Llop LA, Fleta J, Morellon MP, Bueno M. Body mass index, triceps skinfold and waist circumference in screening for adiposity in male children and adolescents. Acta Paediatr 2001; 90: 387-92.
14. Sarria A, Garcia-Llop LA, Moreno LA, Fleta J, Morellon MP, Bueno M. Skinfold thickness measurements are better predictors of body fat percentage than body mass index in male Spanish children and adolescents. Eur J ClinNutr 1998; 52: 573-6.
15. Turconi G, Guarcello M, Maccarini L, Bazzano R, Zaccardo A, Roggi C. BMI values and other anthropometric and functional measurements as predictors of obesity in a selected group of adolescents. Eur J Nutr 2006; 45: 136-43.
16. Chan DFY, Li AM, So HK, Yin J, Nelson EAS. New skinfold-thickness equation for predicting percentage body fat in Chinese obese children. HK J Pediatr 2009; 14: 96-102.
17. Ogechi UP, Akhakhia OI, Ugwunna UA. Nutritional status and energy intake of adolescents in Umuahia Urban, Nigeria. Pak J Nutr 2007; 6: 641-6.
18. Senbanjo IO, Oshikoya KA, Olutekunbi OA, Njokanma OF. Body fat distribution of children and adolescents in Abeokuta, Southern Nigeria. Am J Phys Anthropol 2013; 150: 647-54.
19. Haas GM, Liepold E, Schwandt P. Percentile curves for fat patterning in German adolescents. World J Pediatr 2011; 7: 16-23.
20. Addo OY, Himes HJ. Reference curves for triceps and subscapular skinfold thickness in US children and adolescents. Am J Clin Nutr 2010; 91: 635-42.
21. Ghosh A, Choudhary S, Chowdhury SD, Ghosh T. Fat and fat-free mass in Nepalese children: an assessment of nutritional status. Eur J Pediatr 2009; 168: 1513-7.
22. Musaiger AO, D\'Souza R. Anthropometric characteristics of Pakistani school children living in Bahrain. J Immigrant Minor Health 2009; 11: 205-14.
23. Ozturk A, Budak N, Cicek B, Mazicioglu MM, Bayram F, Kurtoglu S. Cross-sectional reference values for mid-upper arm circumference, triceps skinfold thickness and arm fat area of Turkish children and adolescents. Int J Food Sci Nutr 2009; 60: 267-81.
24. Jaworski M, Kulaga Z, Pludowski P, Grajda A, Gurzkowska B, Napieralska E, et al. Population-based centile curves for triceps, subscapular, and abdominal skinfold thicknesses in Polish children and adolescents-the OLAF study. Eur J Pediatr 2012; 171: 1215-21.
25. Laurson KR, Eisenmann JC, Welk GJ. Body fat percentile curves for U. S. Children and adolescents. Am J Prev Med 2011; 41: S87-S92.
26. Duarte MO, Ruelas YF, Lopez-Alcaraz C, del Toro-Equihua M, Sanchez-Ramirez CA. Correlation between percentage body fat measured by the Slaughter equation and bio impedance analysis tecnique in Mexican schoolchildren. Nutr Hosp 2014; 29: 88-93.
27. Zhang YX, Wang SR. Changes in skinfold thickness and body composition among children andadolescents in Shandong, China from 1995 to 2010. J Hum Nutr Diet 2012; 26: 252-8.
28. Kromeyer-Hauschild K, Glaber N, Zellner K. Percentile curves for skinfold thickness in 7-to 14 year-old children and adolescents from Jena, Germany. Eur J Clin Nutr 2012; 66: 613-21.
29. Boeke CE, Oken E, Kleinman KP, Rifas-Shiman SL, Taveras EM, Gillman MW. Correlationsamongadiposity measures in school-aged children. BMC Pediatrics 2013; 13: 99.
30. Moreno LA, Mesana MI, Gonzalez-Cross M, Gil CM, Ortega FB, Fleta J, et al. Body fat distribution reference standards in Spanish adolescents: the AVENA study. Int J Obes 2007; 31: 1798-805.
31. Abdulrazzaq YM, Nagelkerke N, Moussa MA. UAE population reference Standard charts for body mass index and skinfold thickness at ages 0-18 years. Int J Food Sci Nutr 2011; 62: 692-702.