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Keywords:

  • body composition;
  • children;
  • adiposity;
  • sex;
  • race

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Objective: To investigate sexual dimorphism and race differences in fat distribution (android/gynoid) before and during puberty.

Research Methods and Procedures: Fat distribution was measured by skinfold thickness and DXA in healthy African-American, Asian, and white subjects (n = 920), divided into pre-, early, and late pubertal groups.

Results: Gynoid fat masses adjusted for covariates were lower in late pubertal compared with prepubertal boys, but were not consistently greater in late pubertal compared with prepubertal girls. Progression of sex-specific fat distribution with increasing maturation was present in Asians only. Among African-American and white subjects, early pubertal boys had greater gynoid fat mass compared with the prepubertal group, whereas early pubertal girls had less gynoid fat mass compared with the prepubertal group. Sexual dimorphism in fat distribution was present in all pubertal groups, except among whites at early puberty. Among girls, Asians had lower gynoid fat than whites and African Americans in all pubertal groups. Among boys, Asians had less gynoid fat by DXA in early puberty and late puberty.

Discussion: Comparison among races demonstrated differences in sexual dimorphism and sex-specific fat distribution with progression in pubertal group. However, in all race groups, the fat distribution of late pubertal boys was more “male” or “android” than prepubertal boys, but late pubertal girls did not differ consistently from prepubertal girls. These findings suggested that the greater sexual dimorphism of fat distribution in late puberty compared with prepuberty may be attributable to larger changes in boys with smaller changes in girls.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Fat distribution is recognized as a risk factor for cardiovascular disease in both adults (1, 2, 3) and children (4, 5, 6). An android, or male fat pattern, with relatively greater fat in the upper body region, is associated with negative metabolic predictors (5, 6, 7, 8). A gynoid, or female fat pattern, with relatively greater fat in the hip and thigh areas, is associated with less metabolic risk (9). Although sex-specific patterns of fat distribution had been previously thought to emerge during puberty (10, 11, 12, 13), our recent report describes sex and race differences in fat distribution in a cohort of prepubertal children (14). Identification of potential sex and race differences is of clinical importance because the implications of a specific body composition pattern may differ by sex and race (6, 15).

We have observed race differences in fat distribution among prepubertal Asians, African Americans, and whites (14). Previous reports in adolescents have suggested significantly smaller hip circumferences in Asian females at all pubertal stages compared with whites and Hispanics (16) and greater trunk subcutaneous fat in Asian females compared with whites (17). Differences in subcutaneous fat mass and fat distribution in Asian compared with white adults have also been described (18). To our knowledge, sex- and race-specific fat distribution has not been evaluated at all stages of puberty in a multiracial population of children and adolescents. Understanding the sex- and race-specific effects of puberty on regional body composition may help delineate the developmental timing of specific health risk associations (19, 20).

The aim of this study was to evaluate whether the effect of puberty on fat distribution differs by sex and race. Two independent methods of assessing fat distribution, anthropometry and DXA, were used to investigate relative gynoid fat mass in 920 healthy children and adolescents.

Research Methods and Procedures

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Subjects

Subjects were 442 girls (145 African American; 161 Asian; 136 white) and 478 boys (128 African American; 184 Asian; 166 white) enrolled in a cross-sectional body composition study. Ages ranged from 5 to 18 years, and 39% (358 of 920) were prepubertal. Volunteers were recruited through local newspapers, announcements at schools and after-school centers, and by word of mouth. Consent was obtained from each volunteer's parent or guardian, and assent was obtained from each volunteer. Race was determined by consistent background of both parents and four grandparents by questionnaire using the categories: Asian, non-Hispanic African American, or non-Hispanic white. Participants whose backgrounds did not meet these criteria were excluded from the analysis. The Asian volunteers were of Chinese and Korean background. There were no height or weight restrictions for entry into the study. A medical history from the parent or guardian and a physical examination confirmed normal health status. The Institutional Review Board of St. Luke's-Roosevelt Hospital Center approved the study.

Body Composition Measurement

All medical and body composition evaluations were carried out on the same day at least 1 hour after subjects ate a light meal and while they wore a hospital gown and foam slippers.

Anthropometry

Body weight was measured to the nearest 0.1 kg (Weight Tronix, New York, NY) and height to the nearest 0.5 cm using a stadiometer (Holtain; Crosswell, Wales, United Kingdom). Skinfold thicknesses were measured to the nearest 1.0 mm with a Lange caliper (Beta Technology, Inc., Cambridge, MD) at the following sites: chest, subscapular, abdomen, and thigh. All skinfold measurements were taken on the right side of the body using the procedures recommended by Lohman et al. (21). The average of two readings was recorded with the measurement to ±2 mm. Subjects were measured by one of two examiners (J.W. and Svetlana Kolesnik) during the study period. The intraclass correlation coefficients between the two examiners for skinfold measurement were 0.99 (chest), 0.92 (subscapular), 0.99 (abdomen), and 0.95 (thigh). The skinfold measurement used to define android and gynoid fat masses are presented in Table 1.

Table 1. . Models used to explore whole body fat distribution
Model*Dependent variableIndependent variable
  • *

    Age, height, and weight (covariates); sex, race, and pubertal group (factors).

Skinfold ModelGynoid (sum of abdomen and thigh)Android (sum of chest and subscapular)
DXA ModelGynoid (sum of pelvis and legs)Android (sum of ribs and spine)

DXA

Total body fat, total body fat free mass, regional fat, and regional fat free mass were measured with a whole-body DXA scanner (DPX, Lunar Corp., Madison, WI) using Pediatric Software Version 3.8G (Lunar Corp., Madison, WI).

Repeated daily measurements in three adult subjects showed coefficients of variation (CVs)1 of 5% for arm fat, 1% for leg fat, and 2% for trunk fat. Reproducibility of DXA in children has been reported (22); however, due to concerns surrounding unnecessary radiation exposure in healthy children, scan reproducibility in children was not performed in our study.

The calculation of regional soft tissue mass has been described previously (23). The DXA regions used to define android and gynoid fat masses are presented in Table 1.

An anthropomorphic spine phantom made up of calcium hydroxyapatite embedded in a 17.5 × 15 × 17.5 cm lucite block was scanned for quality control on each working day before subject evaluation. The phantom was also scanned immediately before and after all DXA system manufacturer maintenance visits. The measured phantom bone mineral density was stable throughout the study period at 1.166 to 1.196 g/cm2. Monthly, ethanol and water bottles (8 liter volume), simulating fat and fat-free soft tissues, respectively, were scanned as soft-tissue quality control markers. The ranges in measured R values over the study period were 1.255 to 1.258 (CV = 0.127%) and 1.367 to 1.371 (CV = 0.103%) for ethanol and water, respectively.

Pubertal Staging

Pubertal status was established by the criteria of Tanner (24) for breasts in girls, for genitalia in boys, and for pubic hair in boys and girls, as previously described (25). Pubertal assessment was performed by the pediatric endocrinologist or study nurse in younger subjects, but by self-assessment in volunteers 11 years and older (26). Fasting blood samples for testosterone (boys), estradiol (girls), and gonadotropins (boys and girls) were obtained in a subset of 105 boys and girls in Tanner stages 1 to 5. Results were consistent with pubertal stage assessed by physical examination in 99 cases and were inconsistent for 6 boys in Tanner stages 2 to 3. For the purpose of analyses, subjects were subdivided into three pubertal groups [i.e., prepuberty (Tanner stage 1), early puberty (Tanner stages 2 and 3), and late puberty (Tanner stages 4 and 5)].

Statistical Analysis

Fat distribution has frequently been expressed as ratios (12, 17). In this study, we used the analysis of covariance with gynoid fat as the dependent variable and other relevant variables as covariates (Table 1). Android fat was treated as a covariate, and other covariates included age, weight, and height. This approach was chosen to avoid the numerous problems associated with the use of ratios in statistical analysis (27). Analysis of covariance was used to explore the following: 1) pubertal group (i.e., pre-, early, and late pubertal) differences in body fat distribution within sex by race; 2) sex (boy or girl) differences within pubertal group by race; and 3) race differences (i.e., Asians compared with African Americans and whites) in body fat distribution within pubertal group by sex.

In the regression models, to achieve normal distribution of the residuals, log transformation was used for both dependent variables and weight. Due to the large number of variables considered in each model, p < 0.01 was set as the level for statistical significance. To explore race, sex, and pubertal stage interactions, least-square mean (LS-mean) values were computed for each dependent variable. Adjusted multiple post hoc comparisons (p < 0.01) were used to evaluate the differences in adjusted means. All statistics were computed using SAS software version 8 (28).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

The mean and SD values for age, height, weight, and fat mass of android and gynoid regions measured by skinfold thickness and DXA were computed for each race and sex in three pubertal groups (Table 2). For the total sample, significant interactions were found for sex × race × pubertal group, sex × race, and sex × pubertal group (data not shown). Therefore, differences were explored by comparing adjusted mean values for gynoid fat mass for each sex-race- pubertal group derived from analysis of covariance. The LS-mean of gynoid fat mass log-transformed values for three pubertal groups (pre-, early, and late puberty) within sex for each race group are presented in Table 3. The LS-mean values by sex within race for the three pubertal groups are presented in Figure 1.

Table 2. . Subject characteristics*
    Skinfold thickness (mm)DXA fat mass (kg)
 Age (year)Height (cm)Weight (kg)GynoidAndroidGynoidAndroid
  • *

    Values are presented as mean (SD).

Prepuberty       
 African American       
  Boys (n = 42)7.8 (1.6)131.1 (11.3)32.4 (12.1)29.6 (25.4)18.7 (17.5)3.9 (4.2)1.5 (2.2)
  Girls (n = 52)7.8 (1.5)129.5 (10.0)30.3 (8.4)33.0 (18.0)16.9 (12.4)4.3 (3.1)1.4 (1.8)
 Asian       
  Boys (n = 74)8.1 (1.5)131.6 (9.9)31.8 (8.6)36.5 (19.1)22.6 (14.9)3.9 (2.3)1.7 (1.5)
  Girls (n = 69)7.8 (1.4)127.2 (8.7)27.7 (6.9)33.5 (15.8)20.5 (12.7)3.7 (2.1)1.4 (1.4)
 White       
  Boys (n = 66)7.9 (1.6)131.3 (10.8)30.8 (10.0)29.9 (20.1)16.3 (14.3)3.4 (2.7)1.3 (1.6)
  Girls (n = 55)8.2 (1.5)130.5 (11.0)29.6 (9.2)34.0 (17.4)16.2 (12.7)3.9 (2.7)1.3 (1.7)
        
Early puberty       
 African American       
  Boys (n = 38)12.0 (1.7)156.3 (11.7)53.1 (16.2)41.5 (34.6)25.4 (24.4)6.9 (6.6)3.2 (3.8)
  Girls (n = 34)11.1 (2.1)154.3 (9.6)51.4 (14.0)46.1 (24.6)27.4 (19.1)8.5 (5.6)3.7 (3.0)
 Asian       
  Boys (n = 66)12.5 (2.3)157.1 (13.9)52.9 (14.3)39.7 (20.9)27.3 (17.0)6.0 (3.6)3.2 (2.5)
  Girls (n = 47)12.0 (2.3)150.4 (7.5)45.9 (10.4)48.8 (17.9)29.0 (15.5)6.9 (3.2)3.5 (2.2)
 White       
  Boys (n = 57)11.8 (1.9)153.6 (11.6)47.7 (16.5)41.2 (26.6)23.0 (18.8)6.3 (5.2)2.8 (3.0)
  Girls (n = 48)11.7 (1.4)153.1 (8.3)46.9 (10.2)45.1 (20.6)23.9 (15.2)7.0 (3.7)3.1 (2.2)
        
Late puberty       
 African American       
  Boys (n = 48)15.0 (2.0)172.6 (11.1)67.8 (18.2)28.5 (22.3)19.6 (13.7)6.1 (5.7)2.9 (3.4)
  Girls (n = 59)14.7 (2.1)162.0 (6.8)65.6 (17.9)59.8 (30.0)34.6 (21.0)12.1 (7.2)5.6 (3.9)
 Asian       
  Boys (n = 44)16.1 (1.4)171.6 (5.7)65.5 (12.7)32.1 (17.7)22.8 (14.0)5.7 (3.7)3.6 (2.7)
  Girls (n = 45)15.4 (1.8)160.0 (6.7)58.2 (11.3)56.6 (18.6)35.7 (14.1)9.7 (3.9)5.1 (2.3)
 White       
  Boys (n = 43)15.5 (1.7)173.2 (10.6)67.4 (12.2)30.5 (19.9)20.5 (13.6)6.1 (3.8)3.0 (2.5)
  Girls (n = 33)14.9 (1.7)163.2 (8.4)61.1 (9.8)59.8 (18.7)30.5 (12.9)11.0 (4.5)5.1 (2.4)
Table 3. . Adjusted means of log-transformed gynoid fat at pre-, early, and late puberty*
 PrepubertyEarly pubertyLate puberty
  • *

    The gynoid fat value was adjusted for age, weight, height, and android fat.

  • Significant difference (p < 0.01) for the comparison between prepuberty and late puberty only.

Boys   
 Gynoid skinfolds (mm)   
  African American3.343.423.29
  Asian3.543.493.44
  White3.443.513.17
 Gynoid DXA fat (kg)   
  African American1.581.471.43
  Asian1.511.451.35†
  White1.481.551.31
    
Girls   
 Gynoid skinfolds (mm)   
  African American3.593.563.60
  Asian3.563.723.69
  White3.633.593.63
 Gynoid DXA fat (kg)   
  African American1.831.651.66
  Asian1.601.601.69
  White1.631.561.64
image

Figure 1. Adjusted means and SE of log-transformed values for skinfold-derived gynoid fat and for DXA-derived gynoid fat at three pubertal stages. Adjusted multiple post hoc comparisons were used to evaluate the sex differences (symbol a, p < 0.01) in adjusted means within each race group and race differences (symbol b, p < 0.01) in adjusted means within each sex.

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Pubertal Group Differences in Body Fat Distribution within Sex by Race

In boys within race, the lowest adjusted gynoid fat mass (i.e., consistent with the classic male pattern of fat distribution) was present in the late puberty group in all models (Table 3). However, a progressive decrease in gynoid fat from prepuberty to late puberty was seen only in Asians by the two independent measures (skinfolds and DXA). In contrast, the early puberty group of African-American boys had greater adjusted gynoid fat mass by skinfolds compared with prepubertal African-American boys, and this was seen by both skinfolds and DXA in early pubertal compared with prepubertal white boys.

In girls, the differences between pre- and late pubertal groups were less consistent. Considering results from both skinfolds and DXA models, the highest adjusted gynoid fat mass (i.e., resembling the classic female pattern of fat distribution) was seen in late pubertal Asians only. In African Americans, the greatest adjusted gynoid fat masses by DXA were seen in the prepubertal group rather than in the late pubertal group (p < 0.01). Consistent with findings in Asian boys, the comparison among pubertal groups demonstrated a different pattern for Asian girls compared with the other two race groups. The adjusted gynoid fat masses in early pubertal Asian girls were larger than prepubertal girls by skinfolds, but not different by DXA. Early pubertal African-American and white girls had consistently lower gynoid fat masses than prepubertal girls.

Sex Differences in Fat Distribution within Pubertal Group by Race

Adjusted means and SE of log-transformed values for skinfold-derived gynoid fat and for DXA-derived gynoid fat at three pubertal stages are presented in Figure 1. Adjusted multiple post hoc comparisons were used to evaluate the sex differences (Figure1, symbol a; p < 0.01) in adjusted means within each race group.

In Asians, sex differences in fat distribution were evident in all three pubertal groups with greater gynoid fat in girls than in boys by both the skinfold and DXA models, although the difference in skinfold model at prepuberty was not statistically significant. In African Americans, sex differences in gynoid fat measured by both skinfolds and DXA were observed in all three pubertal groups, with girls having greater gynoid fat deposits than boys (p < 0.01). In whites, sex differences in gynoid fat by both methods were evident in prepuberty (p < 0.01), absent in early puberty, but present in late puberty (p < 0.01).

Race Differences in Fat Distribution within Pubertal Group by Sex: Asians Compared with the Other Two Race Groups

Adjusted means of log-transformed values for skinfold-derived gynoid fat and for DXA-derived gynoid fat at three pubertal stages are presented in Figure 1. Adjusted multiple post hoc comparisons were made to evaluate race differences (symbol b, p < 0.01) in adjusted means within each sex.

Among girls, race differences were more evident in the pre- and late puberty groups compared with early puberty. Asians had statistically less gynoid fat than whites by both skinfolds and DXA at late puberty and by skinfolds at prepuberty. The differences between Asians and African Americans were more apparent by DXA than skinfolds. Asians had less adjusted gynoid fat mass by DXA than African Americans in all pubertal groups, although the difference was not statistically significant in early puberty.

Among boys, the differences between Asians and the other two race groups were not consistent. Asians had statistically less gynoid fat than whites in early puberty, as measured by skinfolds and DXA, and in late puberty, as measured by DXA. Compared with African Americans, Asians had more gynoid fat by skinfolds at prepuberty (p < 0.01) and less gynoid fat by DXA at late puberty (p < 0.01).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

This cross-sectional comparison of pubertal groups in 920 African-American, Asian, and white boys and girls demonstrated that the effect of the progression of puberty on fat depots was greater in boys than in girls. Although late pubertal boys were clearly more “male” with less adjusted gynoid fat mass compared with prepubertal boys, late pubertal girls were not consistently different from prepubertal girls who already showed an adult female fat pattern. This suggests that the sexual dimorphism of fat distribution in late puberty compared with prepuberty is attributable to greater changes in boys with smaller changes in girls.

Second, these data demonstrated a race difference in the course of sex-specific fat distribution with the progression of puberty. Asians had progressively greater gynoid fat mass in girls and less gynoid fat mass in boys, although this was again most evident in boys. A different non-linear pattern was seen in the comparison of the early pubertal group with the prepubertal group in African American and white subjects—early pubertal boys were less “male” (i.e., more gynoid fat) and early pubertal girls were less “female” (i.e., less gynoid fat).

Third, there was generally less gynoid fat in Asians compared with African Americans and whites, especially in girls. These results were based on two different measures of body fat distribution: DXA and skinfolds. Like all in vivo body composition methods, both are indirect and based on assumptions. Each measures a different endpoint: DXA is a measure of total fat and estimates all body fat in a given region, whereas skinfold thickness measures only subcutaneous fat at a specific place of the body. The use of two independent methods strengthened our findings. The general consistency of the comparison between pre- and late pubertal groups within sex and race suggested sex differences in the influence of puberty on these models of fat distribution.

Sex Difference in the Effect of Puberty on Fat Distribution

Although the characteristics of male and female body composition have generally been attributed to gonadal steroids and frequently reported to appear during adolescence, this is not the first study to demonstrate a dramatic effect of puberty on sex-specific fat distribution in boys, but minimal change in girls (12, 29, 30, 31). Unique to this study was the observation that comparisons among pubertal groups did not reveal a steady progression of sex-specific fat distribution with increasing maturation. Early pubertal African-American and white boys had greater adjusted gynoid fat compared with the prepubertal group, whereas African-American and white girls had the opposite pattern. Thus, the difference between pre- and early pubertal groups was discordant from the “expected” sex-specific direction, in spite of physical findings consistent with breast and genital stages 2 and 3, indicating greater concentrations of gonadal steroids (32, 33).

Multiple hormones and other factors influence fat mass and distribution, but adipose tissue has receptors for estrogen, androgen, and progesterone (34, 35). Although expression of receptors and the action of hormones are site- and sex-specific, and local hormone concentrations in adipose depots may differ from circulating levels, in vitro studies in preadipocytes from subcutaneous and visceral depots from men and women have demonstrated increased rates of proliferation with estradiol but not with dihydrotestosterone (35). The pattern of decreased gynoid fat depots compared with prepuberty was seen in early pubertal girls, a period that has been reported to have “relative hyperandrogenicity” with high levels of androgens relative to estrogens (36). The pattern of greater adjusted gynoid masses seen in early pubertal boys compared with prepuberty also coincides with a period of relatively greater estradiol concentration in boys, whereas dramatically lower gynoid fat masses were present in the late pubertal group when testosterone levels are higher (37). In contrast, the adjusted gynoid fat masses in late pubertal girls with higher estrogen levels did not differ from prepubertal girls, suggesting that greater levels of estrogen may not influence these fat depots as much as androgens.

Another cross-sectional study using DXA in subjects from 8 to 27 years of age has suggested a more android or central pattern of fat distribution in girls with advance in maturation (38). This is in contrast to the pattern seen in girls in the current study (a maximum age of 18 years), except in late pubertal African Americans, who had significantly less gynoid fat by DXA compared with the prepubertal group. Increased central adiposity in women has been associated with relative androgen excess, and a decrease in subcutaneous fat with an increase in the visceral fat depot has been observed in female-to-male transsexuals treated with long-term testosterone therapy (39, 40, 41, 42). The dramatic effect of advancing pubertal stage on sex-specific fat distribution in boys, but not girls, and the central fat pattern in girls and women with conditions accompanied by high levels of androgen suggest that testosterone is the mediator. The lack of a difference in these fat depots between pre- and late pubertal girls in our study suggested that, unlike the bone effects of physiological levels of estrogen in men (43), late female pubertal levels of testosterone circulating together with estrogen and progesterone did not affect fat depots. Of interest, although a change to a more female pattern of fat distribution has been seen in male-to-female transsexuals, these individuals were treated with both estradiol and the antiandrogen cyproterone acetate, suggesting that the effects may be, in part, secondary to lack of testosterone, not the presence of estradiol (44). Finally, the hormonal mechanisms for male compared with female fat distribution during puberty may be different from those observed in adulthood because, as shown by in vitro studies of bone, the response to a specific concentration of hormone may vary with the pubertal status of the individual (45).

Race Differences in the Progression of Sex-Specific Fat Distribution and in Fat Distribution

The comparison between pubertal groups suggested a steady progression toward greater sexual dimorphism in the Asian participants, but not in the African-American and white subjects. Indeed, the relative gynoid fat masses of boys and girls in the African-American and white early pubertal groups were “less male” and “less female,” respectively, so that sexual dimorphism was less evident than in the prepubertal group. The implied race difference in the “course” of fat distribution toward adult male and female patterns has not been previously described. Although race differences in circulating hormones have been reported in adults and adolescents (46, 47, 48), the investigators were not evaluating fat distribution.

The mechanism of the observed race differences in the comparison between pubertal groups needs further exploration. However, these differences are the further evidence of race, sex, and pubertal group specificity of body composition. All of these factors must be considered in defining phenotypes for investigation of health implications.

Limitations

This study was limited by its cross-sectional design. Ideally, elucidation of the effects of puberty on features of interest should be based on serial measures of the same individuals as they progress through puberty. Another limitation of this study was the fact that hormone levels were available only in a subset of subjects, and, therefore, pubertal status could not be confirmed biochemically in all subjects. Nevertheless, the high agreement with pubertal classification seen in this subset makes it unlikely that misclassification was an important factor.

In conclusion, the effect of puberty on these models of sex-specific fat distribution was much greater in boys than girls, so that late pubertal boys were clearly different from prepubertal boys, whereas this was not the case in girls. This suggested that pubertal estrogen may not be the mediator of a female pattern of fat distribution. The observed sex, race, and pubertal differences emphasized the importance of including these factors in the definition of phenotypes for investigation of the associated health risks.

Acknowledgment

  1. Top of page
  2. Abstract
  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

This study was supported, in part, by National Institutes of Health Grants DK-37352, HD-42187, and HL-70298.

Footnotes
  • 1

    Nonstandard abbreviations: CV, coefficient of variation; LS-mean, least-square mean.

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  3. Introduction
  4. Research Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References
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