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O A RIGINAL RTICLES
1884 Journal of Applied Sciences Research, 9(3): 1884-1891, 2013 ISSN 1819-544X This is a refereed journal and all articles are professionally screened and reviewed ORIGINAL ARTICLES Adiponectin and Adiposity Indices among Obese Primary School Children 1 Nayera E Hassan, 1Sahar A El-Masry, 1Muhammad Al-Tohamy, 1Salwa El-Batrawy, 2Ahmed W. Abou-Zeid, 3Mona Anwar 1 Biological Anthropology Department, Medical Research Division, National Research Centre, Egypt Oral Histopathology Department, Faculty of Dentistry, Misr International University, Egypt 3Special Needs Department, Medical Research Division, National Research, Centre, Egypt 2 ABSTRACT Background: Adiponectin is the most abundant hormone exclusively produced by adipose tissue and influenced by obesity. Objectives: to verify the impact of obesity on adiponectin levels in pre-pubertal children and to find out the correlation between adiponectin levels, body composition and lipid profile. Subjects and methods: 68 obese children, aged 9.96 + 1.32 years, were included in this study. Complete clinical examination, anthropometry (body weight, height, waist and hip circumferences and skinfold thickness) and body composition assessment (Fat %, fat mass “FM” and fat free mass “FFM”) were attempted. BMI, Waist/Hip ratio, and peripheral and central adiposity were calculated. Serum adiponectin, total cholesterol (TC), triglycerides (TG), high-density lipoprotein-cholesterol (HDL-C), low-density lipoprotein-cholesterol (LDL-C) and TC/HDL-C were measured. Results: Prevalence of obesity and overweight were 3.7%, 7.7% in boys and 7.6%, 12.6% in girls, respectively. Mean plasma concentrations of triglycerides (both sexes), LDL-C (boys) were above those considered normal for age, while HDL-C (boys) and adiponectin (both sexes) were lower. Impaired total cholesterol, LDL-C, HDL-C and high WC were more prominent among boys, while impaired triglycerides was more prominent among girls. Low adiponectin level was detected among the whole sample; boys and girls. For boys, negative significant correlations were detected between adiponectin and weight, BMI, waist and hip circumferences, subscapular SF, fat %, triglycerides and TC/HDL-C, while detected only with biceps SF and TC/HDL-C for girls. Conclusion: The inverse relationship between plasma adiponectin concentrations and some adiposity markers, in obese children, was dependant on the sex in prepubertal age. Key wrods: Adiponectin, anthropometry, body composition, lipid profile, children. Introduction In the past few decades, as a result of modern lifestyles, the prevalence of obesity is dramatically increasing worldwide in both children and adults (Panagiota et al., 2012). Hence, obesity has become the major complex and growing global childhood health problem, which poses a significant economic burden to both developed and developing countries (Anne et al, 2008). In Egypt, the prevalence of obesity is 8.0% among Egyptian school students; however, the prevalence of overweight is 11% (Hassan et al., 2011). Adiponectin is an adipokine that has drawn much more attention recently. It is one of the most studied adipokines in neonates, children, and adults (Panagiota et al., 2012). It is expressed and secreted exclusively by differentiated adipocytes with larger amounts secreted from subcutaneous than from visceral fat (Zhang et al., 2011; Hasani-Ranjbar et al., 2012). It has been reported that increased body adiposity in childhood is an important risk factor for hypoadiponectinmia in adulthood (Toprak et al., 2011). Low adiponectin levels, during childhood or adolescence, could have negative long-term health effects (Emken et al., 2010).It can be a predictor of adverse health outcomes such as cardiovascular disease, type II diabetes and cancer in adults, Adiponectin level that decreases in obesity and related diseases pathology (Shargorodsky et al., 2009), might be a valuable biomarker for identifying non-overweight children at risk for later metabolic issues (Jie et al., 2010). So, the purpose of this research is to verify the impact of obesity on adiponectin levels in pre-pubertal children and to find out the correlation between adiponectin levels, body composition and lipid profile. Materials and Methods Subjects: Corresponding Author: Sahar A El-Masry, Biological Anthropology Department, Medical Research Division, National Research Centre, Egypt E-mail: masrysa@yahoo.com 1885 J. Appl. Sci. Res., 9(3): 1884-1891, 2013 The study group consisted of 68 obese children (32 boys and 36 girls), aged 9.96 + 1.32 (range 6.5-11.5 years). They were derived from a cross-sectional survey, conducted on 2083 child (874 boys and 1209 girls), from 2 primary public schools, randomly selected, situated in Giza governorate, Egypt, during the period of October 2009 to April 2010. These children were required to meet the following inclusion criteria: age, 7-11 years and BMI greater than the 95th percentile for age and sex based on the Egyptian Growth Reference Charts (Ghali et al., 2008). Pupils were excluded if they had a prior major illness, including type 1 or 2 diabetes, received medications or had a condition known to influence body composition, insulin action or insulin secretion (e.g. glucocorticoid therapy, hypothyroidism and Cushing’s disease). Prior to enrollment, permission to perform the study was granted by the Ministry of Education, and the directors of the school included in the research. Parents were fully informed about the purpose and methods of the study and signed a written consent. The children provided their verbal assent. Approval to conduct this survey was granted by the "Ethical Committee" of the “National Research Centre”. All information and blood samples were collected by a well-trained staff during morning visits to the schools. Anthropometric assessment: Each child underwent a complete physical examination, including anthropometric measures. Height, weight, waist and hip circumferences and skinfold thickness were measured following the recommendations of the International Biological program (Hiernaux and-Tanner, 1969). Height was measured to the nearest 0.1 cm on a Holtain portable anthropometer, and weight was determined to the nearest 0.01 kg using Seca Scale Balance, with the subject wearing minimal clothing and no shoes. Waist circumference (central adiposity) was measured at the level of the umbilicus with the subject standing and breathing normally, hip circumference at the level of the iliac crest, using non-stretchable plastic tape to the nearest 0.1 cm. Skinfold thicknesses were taken at five sites: triceps, biceps, sub scapular, suprailiac and abdominal. Each skinfold was measured three times on the left side of the body; with Holtain skin fold caliper to the nearest 0.2 mm, and the mean value was recorded. The following adiposity indices were calculated: Body mass index (BMI): as weight (kg) divided by height (m)2. BMI was used for subject’s classification as normal weight [<85th percentile], overweight [ > 85th percentile], and obese[> 95th percentile]. BMI was also expressed in terms of standard deviation scores (z-scores), using the Egyptian Growth Reference Charts (Ghali et al, 2008) Waist/ Hip ratio (cm/cm). Peripheral adiposity: as the sum of triceps and biceps skinfold thickness. Central adiposity: as the sum of sub scapular, suprailiac and abdominal skinfold thickness. Body Composition: Whole body resistance and reactance (capacitance) were measured using a Bioelectrical Impedance Analyzer (HOLTAIN LIMITED). As specified by the manufacturer, the unit was calibrated before testing using 400-ohm resistor, and electrodes were placed on right wrist and ankle. By using pupil’s sex, age, weight and height approximated to the nearest unit, the percentage body fat (Fat %), fat mass (FM) and fat free mass (FFM) were derived. Biochemical assessment: Early morning forearm venous blood samples (10 ml) were obtained from each child; before breakfast; for biochemical screening tests after 12-hours overnight fasting. Professional staff performed venipuncture. The blood samples were left to clot; sera were separated by centrifugation for 10 minutes at 5000 rpm then stored at -80 ºC until assays. Serum adiponectin levels were measured using commercially available Enzyme Linked Immunosorbent Assay (ELISA) kits, provided by AviBion Orgenium Laboratories, Finland. Serum concentrations of total cholesterol (TC), triglycerides (TG) and high-density lipoprotein-cholesterol (HDL-C) were measured using commercially available kits provided by STANBIO Laboratory Inc. (1261 North Main Street Boerne Texas 78006 USA). LDL-C was calculated according to an equation developed by Friedewald et al., 1972 as follows: LDL-C= Total cholesterol –Triglycerides/5+ HDL-C. The ratio between total cholesterol and high-density lipoprotein-cholesterol (TC/HDL-C) was calculated. Definitions: * High WC: If WC > 90th percentile for age and sex (WHO, 1999). 1886 J. Appl. Sci. Res., 9(3): 1884-1891, 2013 * Dyslipideamia: Any of the following: a. high triglycerides [>110 mg/dL] b. low HDL-cholesterol [<40 mg/dL]. c. high total cholesterol [>210 mg/dL]. * High LDL–Cholesterol [> 130 mg/dL] according to Grundy et al., 2004. * Low adiponectin [> 3.5 μg / mL ] according to (Nien et al, 2007). Statistical Analysis: Data were reported as means ± standard deviations (SD) or as proportions (%). The results were evaluated on the basis of age-specific recommended normal range values for biochemical parameters (WHO, 1999). Statistical evaluation of the results was performed with the SPSS computer program, version 16.0. Student's independent t test was used to examine the sex differences. Pearson’s correlation coefficients were used to assess relationships between independent variables. The level of significance was set at a probability of less than 5% (p<0.05). Results: The survey; from which the present study was conducted; revealed that prevalence of obesity among 2083 primary school children was 6.0% (3.7% in boys and 7.6% in girls); their mean age was 9.83+1.43 years. However, the prevalence of overweight (BMI lies between 85th and 95th percentile for age and gender based on the Egyptian Growth Reference Charts) was 10.5%; 7.7% in boys and 12.6% in girls. Anthropometric Characteristics: Although girls was significantly heavier than boys (p= 0.026), BMI-Z score, waist and hip circumferences, waist/hip ratio and body composition parameters did not differ significantly between genders. However, there were highly significant gender differences in skinfold thickness, where girls had higher values in subscapular skinfold thickness and boys had the higher values of biceps and abdominal skin fold thickness and peripheral fat (table, 1). Biochemical Profile: Mean plasma concentrations of triglycerides (for both sexes), LDL-C (for boys) were above those considered normal for age, while HDL-C (for boys) and adiponectin (for both sexes) were lower than those considered normal for age according to WHO, 1999. On the other hand, mean total cholesterol (for both sexes), as well as, HDL-C and LDL-C for girls were within the acceptable range. However, insignificant gender differences were detected regarding all the biochemical profile (table, 2). The proportion of children with impaired concentrations of lipid profiles and adiponectin, revealed that impaired total cholesterol, LDL-C, HDL-C and high WC were more prominent among boys, while impaired triglycerides was more prominent among girls. Low adiponectin level was detected among the total sample; boys and girls (table, 3). Correlation between serum adiponectin and whole body composition, fat distribution and lipid profile by sex are presented in table 4. For boys, adiponectin had significant negative correlations with body weight, BMI, WC, hip C, subscapular SF, fat%, triglycerides, and TC/ HDL-C, and significant positive correlations with fat free mass and HDL-C. However, for girls, adiponectin had significant negative correlations only with biceps skinfold thickness and TC/ HDL-C. Table 1: Anthropometric characteristics and body composition by sex Parameters Boys (N = 32) Mean +SD Age 9.81 +1.23 Weight (Kg) 53.75 +12.50 Height (cm) 140.40 +9.82 BMI-Z Score 2.51 +0.41 Waist C (cm) 78.91 +8.34 Hip C(cm) 91.93 +8.40 Waist/Hip ratio 0.86 +0.04 Skinfold (mm) Triceps 27.25 +4.62 Biceps 20.63 +4.74 Subscaular 23.93 +3.09 Girls (N = 36) Mean 10.09 61.00 145.17 2.66 82.76 95.64 0.87 p +SD +1.40 +13.57 +10.84 +0.57 +14.12 +9.16 +0.20 0.388 0.026* 0.063 0.222 0.171 0.088 0.660 25.07 16.70 26.61 +6.10 +5.63 +4.56 0.119 0.004** 0.009** 1887 J. Appl. Sci. Res., 9(3): 1884-1891, 2013 Suprailiac Abdominal Peripheral fat Central fat Body Composition Fat % Fat mass (Kg) Fat free mass (Kg) 26.50 28.68 47.88 79.10 +4.13 +5.44 +8.34 +11.23 26.57 24.36 41.77 77.53 +6.08 +6.46 +9.50 +14.54 0.961 0.006** 0.010** 0.638 43.39 23.01 35.03 +15.24 +8.70 +6.85 39.10 25.48 38.86 +4.66 +7.62 +7.69 0.165 0.270 0.056 Table 2: Biochemical indices of the study participants by sex Parameters Boys (N = 32) Mean Adionectin 1.80 Lipid profile Triglycride (mg/dl) 125.86 Total Cholesterol (mg/dl) 195.13 HDL-C(mg/dl) 37.77 LDL-C(mg/dl) 132.09 TC/HDL-C 6.41 +SD +0.45 Girls (N = 36) Mean 1.73 p +SD +0.41 0.495 +33.99 +60.94 +15.26 +61.16 +4.02 136.66 182.23 42.31 113.21 5.09 +37.83 +57.93 +19.64 +59.62 +2.44 0.222 0.374 0.298 0.205 0.113 Table 3: Distribution of the children according to the cut offs for normal and abnormal lipid profile and adiponectin Boys Girls Total N (%) N (%) N (%) High WC 28 (87.5) 25 (69.4) 53 (77.9) Lipid Profile: Dyslipideamia 28 (87.5) 34 (94.4) 62 (91.2) HighTriglycerides 20 (62.5) 29 (80.6) 49 (72.1) High Total Cholesterol 16 (50.0) 6 (16.7) 22 (32.4) Low HDL- Cholesterol 20 (62.5) 17 (47.2) 37 (54.4) High LDL- Cholesterol 20 (62.5) 10 (27.8) 30 (44.1) Low Adiponectin 32 (100.0) 36 (100.0) 68 (100.0) Table 4: Correlation between serum adiponectin and whole body composition, fat distribution and lipid profile by sex Adiponectin Boys Girls r p r p Weight (Kg) - 0.516** 0.003 - 0.067 0.698 BMI (Kg/cm²) - 0.410* 0.020 0.024 0.892 BMI-Z Score - 0.188 0.302 0.144 0.404 Waist C (cm) - 0.423* 0.016 0.050 0.774 Hip C(cm) - 0.496** 0.004 - 0.052 0.762 Waist/Hip ratio - 0.010 0.957 0.064 0.709 Skinfold (mm) Triceps - 0.045 0.807 - 0.081 0.675 Biceps - 0.143 0.435 - 0.429* 0.020 Subscaular - 0.418* 0.017 - 0.098 0.612 Suprailiac - 0.083 0.650 0.032 0.868 Abdominal - 0.157 0.390 0.093 0.631 Peripheral fat - 0.106 0.563 0.202 0.293 Central fat 0.008 0.966 0.024 0.901 Fat % - 0.523** 0.004 0.048 0.813 Fat mass (Kg) 0.366 0.055 - 0.092 0.649 Fat free mass (Kg) 0.449* 0.017 0.209 0.296 Triglycerides - 0.397* 0.025 0.002 0.992 Total Cholesterol 0.082 0.655 0.002 0.989 HDL- Cholesterol 0.470* 0.007 0.326 0.056 TC/HDL-C - 0.402* 0.023 - 0.352* 0.038 LDL- Cholesterol - 0.078 0.672 - 0.120 0.491 Discussion: Adiponectin levels differ with age, sex and obesity. At birth, adiponectin levels are extremely high and fall off gradually until puberty. During pubertal development an additional progressive decline in adiponectin levels occurs mainly in boys, which leads to lower adiponectin levels compared with girls. This decline is strongly associated with androgen levels and accounts for the sex differences seen in adults (Hannah et al., 2009). The present study revealed that plasma adiponectin levels are significantly lower in obese children; males and females; in comparison to those considered normal- weight for age according to WHO , 1999. This agrees with the majority of previous studies which detected an inverse correlation of adiponectin with obesity, in both sexes, at prepubertal or pubertal age (Araki et al., 2010 in Japan; Arslan, et al., 2010 in Turkey; Emken et al., 1888 J. Appl. Sci. Res., 9(3): 1884-1891, 2013 2010 in USA; Patricia et al., 2011 in Mexico; Hassan et al., 2011 in Egypt; Zhang et al., 2011 in China; Atwa et al., 2012 in Egypt; Gherlan et al., 2012 in Romania; Aggeloussi et al., 2012 in Greece; Ochiai et al., 2012 in Japan). In general, adiponectin levels decrease in obese subjects regardless of definition, either by BMI or by WC (Arnaiz et al., 2010 in Chile; Zhang et al., 2011 in China; Hasani-Ranjbar et al., 2012 in Iran), i.e. either with abdominal obesity or with visceral obesity. Sex difference: The results of the current research revealed insignificant sex difference in adiponectin level. Thus, they agree with the findings concluded by Reinehr et al., (2004) in Spain, Araki et al., 2006 in Japan, Valeria et al., (2009) in Italy, Hassan et al., (2011) in Egyp and Patricia et al., 2011 in Mexico. They have reported that, in both prepubertal and pubertal children, no sex difference was found in serum adiponectin level. On the other hand, Madeira et al., 2009 in Portugal; Emken et al., 2010 in USA; Riestra et al., 2011 in Spain; Zhang et al., 2011 in China, have reported that, in younger children, adiponectin levels were significantly higher in girls than in boys. The study of Nishimura et al., 2007, also showed that low level of adiponectin and male sex were significantly correlated. Some authors attributed these ethnic differences in adiponectin level to the effect of both genetic and environmental factors, e.g. Mediterranean diet, enriched in alcohol, nuts, and whole grains, is associated with higher adiponectin concentration (Combs et al., 2003; Panagopoulou et al., 2008). Therefore, such ethnic differences should be taken into account for international comparisons. Anthropometric Characteristics: The present study revealed that, there were insignificant sex differences regarding the studied anthropometric parameters expect in skinfold thickness. Obese girls had highly significant higher values in subscapular skin fold thickness indicating a tendency for central fat distribution and obese boys had highly significant higher values of biceps and abdominal skin fold thickness and peripheral fat, indicating a tendency for both central and peripheral fat distribution. These coincide with the previous studies (Goble et al; 1992; in Macedonia; Mast et al, 1998; in Germany; Gültekin et al., 2005; in Turkey) which confirmed that sexual dimorphism of fat patterning in children is to be seen in the age of 5 - 11 years. These differences are independent of gender differences in body weight. Goble et al; 1992; recorded also insignificant sex differences in the anthropometric measurements of Macedonian elementary school students. The results also showed that, in boys, adiponectin had significant negative correlations with body weight, BMI, WC, hip C, subscapular SF and fat%, and significant positive correlations with fat free mass. However, in girls, adiponectin had significant negative correlations only with biceps skin fold thickness. This comes in concordance with some previous studies (Atwa et al., 2012; Gherlan et al., 2012; Karmeli et al., 2012; Nascimento et al., 2012; Ochiai et al., 2012). They reported that adiponectin levels are significantly, and strongly negatively related to anthropometric parameters such as, body weight, body mass index (BMI), BMI-Z score, waist circumference, waist to hip ratio, intra-abdominal fat and percentage body fat, supporting the evidences that obesity was related to low adiponectin level Karmeli et al., 2012 and Ochiai et al., 2012, in agreement with the current results, stated that, in children and adults, the accumulation of visceral adipose tissue was inversely correlated with adiponectin level. Panagopoulou et al., (2008) also stated that, in obese children, although adiponectin level was significantly negatively correlated with the percent of total body fat, yet this difference did not reach statistical significance except after adjustment for sex. Although, such decreased level of adiponectin has been attributed to the accumulation of visceral fat (Wagner et al., 2008) yet, plasma adiponectin level is not a simple marker of central fat in children (Ong et al., 2006). Zhang et al., 2011, found that low adiponectin levels exist even in the peripheral or abdominal obesity alone and insignificant differences were observed between peripheral and abdominal obesity. Toprak et al., 2011, also stated that childhood skinfold thickness (which represents total body adiposity) and BMI-Z score are obesity determinants for lower adiponectin levels in young adulthood, although these relationships are not independent of adult measures of adiposity. Ochiai et al., 2012, stated that the correlation between adiponectin level and anthropometric variables, in obese subjects (of both genders), were consistently higher than in the non-obese ones On the other hand, some authors found that plasma adiponectin levels were significantly and negatively correlated with BMI in both boys and girls (El-Mesallamy et al., 2011; Nascimento et al., 2012). Other investigators found significant correlations between anthropometric variable and adiponectin levels, among girls only (Ochiai et al., 2012). The different reported correlations between serum adiponectin level and anthropometric parameters, in children and adolescents may be attributed to racial differences and sociocultural eating habits. 1889 J. Appl. Sci. Res., 9(3): 1884-1891, 2013 Biochemical Profile: The results of the present study revealed that there was insignificant sex differences detected regarding all the biochemical profile. The proportion of children with impaired concentrations of lipid profiles and adiponectin, revealed that impaired total cholesterol, LDL-C, HDL-C and high WC were more prominent among boys, while impaired triglycerides was more prominent among girls. Low adiponectin level was detected among the total sample; boys and girls. For boys, adiponectin had significant negative correlations with triglycerides, and TC/ HDL-C, and significant positive correlations with HDL-C. However, for girls, adiponectin had significant negative correlations only with TC/HDL-C. Valeria et al., 2009 and Zhang et al., 2011; in agreement with the current results; stated that, in general, serum adiponectin levels decrease with the increase in the number of metabolic syndrome components. Hulthe et al., 2003, had reported a significant inverse relationship between hypoadiponectinmia, obesity and dyslipidemias. Moreover, it has been concluded that, following lifestyle intervention in obese children, adiponectin proved to be the most significant predictor of improved metabolic profile (Gabriel et al., 2010; Zhang et al., 2011). Atwa et al., 2012, had reported that obese children with metabolic syndrome “MS” have a significantly lower serum adiponectin level compared to obese children without “MS”. On the other hand, Riestra et al., 2011, stated that adiponectin showed a positive correlation with HDL-C in both genders (independently of BMI), and significantly correlated negatively with TG, LDL–C in girls, therefore, adiponectin level is more strongly related to better lipid profile in girls than in boys. Wagner et al., 2008, found that, although a significant correlation was found between high adiponectin levels and high HDL-C or low TG, yet this correlation appears to be independent of body fat or childhood obesity and this may be attributed to the independent effect of adiponectin on lipid metabolism. On the contrast, some investigators found insignificant correlation between adiponectin and HDL-C and TG (Valeria et al., 2009). Conclusion: The inverse relationship between plasma adiponectin concentrations and some adiposity markers, in obese children, was dependant on the sex in prepubertal age. So, low plasma adiponectin level estimation can be considered as a comprehensive biomarker of the metabolic syndrome in childhood obesity, particularly boys. It could preventing its complications, and used as a screening tool, before applying more time-consuming techniques in obese children. References Aggeloussi, S., A.A. Theodorou, V. Paschalis, M.G. Nikolaidis, I.G Fatouros, E.O. 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