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From the Department of Human Nutrition and Division of Epidemiology and Biostatistics, University of Illinois at Chicago, Chicago, Illinois
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Objective. To examine the influence of early SM on fatness in boys and compare it with girls, and to test the hypothesis that the associations differ by gender because of the differences in growth and SM patterns in boys and girls.
Study Design. Cross-sectional study.
Subjects. One thousand five hundred one girls and 1520 boys (aged 8–14 years) who participated in the Third National Health and Nutrition Examination Survey survey (1988–1994) and had complete anthropometry (weight, height, skinfold thickness) and SM data.
Methods. Based on each individual’s age and SM status (Tanner stages: genitalia stages for boys and breast stages for girls), the subjects were classified as: 1) early maturers (those who reached a certain Tanner stage earlier than the median age for that stage), and 2) the others (average and later maturers). Overweight was defined as a body mass index (BMI) 
85th percentile, and obesity 95th percentile. Logistic regression analysis was to test how early maturation affected the risks for overweight and obese. Using multiple linear regression models, the associations between fatness (BMI and skinfold thickness) and SM were systematically examined. Covariates including age, ethnicity, residence, family income, energy intake, and physical activity were adjusted.
Results. Early SM was positively associated with overweight and obesity in girls, but the associations were reverse for boys. The prevalence of overweight in early maturers versus the others was 22.6% versus 31.6% in boys and 34.4% versus 23.2% in girls; the figures for obesity were 6.7% versus 14.8% and 15.6% versus 8.1%, respectively. Odd ratios and 95% confidence intervals for obesity were 0.4 (0.2, 0.8) for boys and 2.0 (1.1, 3.5) for girls, and covariates were adjusted. Most significant differences in overweight and obesity among ethnic groups disappeared after controlling for SM. Fatness (BMI and skinfold thickness) was associated with SM stages and with early maturation in boys and girls, but the associations were in opposite directions. Compared with their counterparts, early maturing boys were thinner, whereas early maturing girls were fatter.
Conclusions. Obesity is associated with sexual maturation in both boys and girls, but the association differs. There is positive association in girls, but a negative one in boys. Maturation status should be taken into consideration when assessing child and adolescent obesity.
Key Words: child • adolescent • fatness • body mass index • obesity • overweight • sexual maturation
Abbreviations: SM, sexual maturation • BMI, body mass index • NHANES III, Third National Health and Nutrition Examination Survey • CDC, Centers for Disease Control and Prevention • SES, socioeconomic status • CI, confidence interval • OR, odds ratio
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Limited research has been conducted in boys and male adults to study the association between SM and obesity. This is particularly attributable to the difficulties of measuring SM in males in epidemiologic research. A systematic examination of the association in boys and comparison of it to girls will provide useful insights to advance our understanding of the controversial relationship between SM and obesity. A good understanding of the relationship between SM and obesity has many important clinical and public health implications. For example, it can help refine and develop appropriate anthropometry references (eg, BMI cutoffs) for child and adolescent obesity13,24,25; second, it can guide the targeting of efforts and resources in the prevention and management of child and adolescent obesity.
Studies from the United States and other industrialized countries and developing countries provide strong evidence of the secular trends of SM among adolescents.26–29 Recently, based on findings from females, some scholars warned that with the secular trends of early maturation, the obesity epidemic in American children and adolescents will become even more alarming. However, it is not clear whether this is true for males. The literature has documented remarkable gender differences in growth and SM patterns, particularly during puberty.26,30,31 Nevertheless, the continuing secular changes in SM observed in the United States and in other populations over the past 2 decades suggest the need to examine their impacts on individuals’ health (eg, obesity) and well-being.
For epidemiologic studies of SM and fatness, a big challenge is to find good measures of SM and appropriate approaches to classify the timing of SM (ie, to categorize early, average, and late maturers). In previous studies, age at menarche was predominately used as the indicator of SM, and as a result, males and girls at young ages could not be included. Although age at menarche has been widely used as an indicator of females’ SM and is easy and cheap to collect,25,26 there are a few additional limitations when using it to study the relationship between SM and fatness. Usually menarcheal age is reported in whole years, and as a result, individuals’ SM cannot be classified precisely (eg, 2 girls are not differentiated if 1 has menarche at the beginning of age X and the other, at the end of age X). In addition, recall errors are of concern. Another major gap in the literature is that most previous studies addressing the influence of SM on obesity fail to adjust for potential confounders such as diet and physical activity.
Using the Third National Health and Nutrition Examination Survey (NHANES III) data collected in the United States during 1988–1994,32 we examined the association between SM and obesity among boys, and compared it with girls. We were able to include both boys and girls, old children (before puberty), and adolescents with our proposed approach of classifying the timing of SM. In addition, we adjusted for potential confounders.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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NHANES III, conducted in 2 phases between 1988 and 1994, was a cross-sectional representative sample of the US civilian noninstitutionalized population aged 2 months and older. NHANES III oversampled blacks, Mexican Americans, children under 5 years of age, and the elderly (60 years). Detailed descriptions of the sample design and operation of the survey are published elsewhere.32 Standardized protocols were used for all interviews and examinations. Data on anthropometry, sociodemographic characteristics, diet (one 24-hour recall), and physical activity were collected for each individual. Maturation status for children aged 8 to 18 years was evaluated by physicians in the physical examination.
Outcome and Independent Variables
Anthropometry
Measures of weight, height, and skinfold thickness (triceps, subscapular, suprailiac, and thigh) were collected. We calculated BMI (= weight[kg]/height[m]2) and the sum of skinfold thickness (= triceps + subscapular + suprailiac + thigh) for each individual.
Definitions of Overweight and Obesity
Because direct measurement of adipose tissue is not feasible in many cases, particularly in population-based research, simple anthropometric indices such as BMI are recommended to classify overweight in children and adults.2,25,33–36 To define overweight and obesity, we used the 2000 Center for Disease Control and Prevention (CDC) growth charts (BMI cutoffs), ie, the 85th percentile for overweight and 95th percentile for obesity.35
Sexual Maturation Status
Data on Tanner stages (pubic hair stages for both sexes, breast stage for girls, and genitalia stages for boys, which were evaluated by physicians in the physical examination) were collected for children and adolescents aged over 8 years, and self-reported age at menarche was collected for girls. We chose to use breast stages (stage 1–5) for girls and genitalia stages (stage 1–5) for boys to classify children’s SM status, because median ages at breast stage 2 and genitalia stage 3 are recommended by a World Health Organization Expert Committee as indicators of SM for international use.25 For children and adolescents of the same age, those at a higher Tanner stage were more advanced in SM status.
Early Onset of Sexual Maturation
Subjects were grouped as "early maturers" if they reached a certain SM stage earlier than the median age for that stage in the population, and otherwise, as "the others" (average and late maturers). For example, a girl would be classified as an early maturer if she was at breast stage 2 and her chronological age was less than the median age for breast stage 2. Using the status quo method with probit analysis, we calculated the median age for each Tanner stage for girls and boys. The status quo method is recommended for calculating median ages of maturation events from cross-sectional data.25,26 Only data on each individual’s chronological age (in years rounded to 0.1 in our analysis) and SM status (eg, breast stage 2: yes or no) were necessary. Compared with retrospective methods based on self-reported menarcheal age, this method suffers from less recall errors. (Note more details about the probit analysis and the results are available from the author at request.) In addition, following the similar procedures, analyses were also conducted using public hair stages. We found a moderate agreement between pubic hair stages and the other 2 SM indicators (breast and genitalia stages) in classifying early and nonearly maturers (the agreement and 
was 77% and 0.48 for girls and, 74% and 0.33 for boys, respectively). This particularly was attributable to the fact that pubic hair stages are a less favorable indicator of SM than the other 2 indicators, which might have resulted in more misclassifications.25
Main Covariates
The following covariates were included in our analysis: 1) age; 2) race and ethnicity: based on self-reported race and ethnicity information, subjects were classified into 4 groups: non-Hispanic white, non-Hispanic black, American Mexican, and other. (Note that race and ethnicity is also likely an indicator of socioeconomic status [SES]); 3) SES: household income was used as an indicator of SES. A measure of family income relative to poverty line (ie, "poverty ratio") was provided by the CDC/National Center for Health Statistics, which allows for appropriate comparisons across regions and groups; 4) energy intake: Total energy intake calculated by the National Center for Health Statistics based on one 24-hour recall. We also examined dietary fat intake (as percentage of energy from fat) but chose not to include it in the final models, because it was not a significant regressor and did not improve model fit; 5) physical activity (answers to "Times per week exercise made you sweat?") and inactivity (answers to "Hours of TV watched yesterday"); and 6) urban versus rural residence. These covariates were tested and controlled for as potential confounders, because studies show that they are risk factors for obesity,2,37 and there is no evidence suggesting that they are the intermediates in the pathway between SM and obesity.
Data Analysis
We first examined the prevalence of overweight and obesity in American boys and girls stratified by their SM status (ie, early maturers and nonearly maturers). Student t tests were performed to test the differences between early and nonearly maturers. Then, with logistic regression we studied the associations between overweight, obesity, and SM (early maturers vs the others). Finally, using multiple linear regression analysis, we examined the association between SM, BMI, and skinfold thickness. All regression analyses were conducted for boys and girls separately and adjusted for age, race/ethnicity, family income, urban-rural residence, total energy intake, physical activity, and inactivity (television viewing time). Collinearity was tested by examining the variance inflation factor. No collinearity was detected, as none of the variance inflation factors was >10.38 In general, the correlation coefficients between the independent variables were small (all <0.2). Furthermore, analyses adjusting for height were run, and results (not presented) were compared with the above results. In general, the 2 sets of findings were consistent, although discrepancies were observed in some cases. Height was not controlled for in the final models, because we suspected that SM affects obesity at least partly because it influences individuals’ linear growth during childhood and adolescence. Data management and data analysis were performed with SAS Version 8.0 (SAS, Cary, NC) and Stata Version 7.0 (Stata Co, College Station, TX). We used Stata survey procedures that accounted for sampling weights to allow generalization of the results to the population of children and adolescents in the United States and to adjust standard errors for cluster sampling.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Association Between Obesity and Early Sexual Maturation
The prevalence of obesity and overweight among boys and girls by SM status was presented in Figs 1 and 2. In general, compared with the average and late maturers, the prevalence of overweight and obesity was lower in early-maturing boys, but higher in early-maturing girls. The differences in the prevalence of obesity were more remarkable than those for overweight. The differences for children in the "other" race/ethnicity category were greater than those for other ethnic groups.
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As shown in Table 3, significant associations were observed between early SM and fatness for both boys and girls. Early-maturing boys had lower BMI and skinfold thickness measures than their counterparts; whereas early-maturing girls had greater measures of BMI and skinfold thickness. We also examined the influence of SM on boys’ and girls’ weight and height, which suggests an interesting gender difference. Early SM was related to increased height but not to increased body weight in boys, while it was associated with both increased height and weight in girls. This suggests that SM might have different biological influences on growth in weight and height in boys and girls, which may help explain the gender differences we observed for the associations between SM and fatness (BMI and skinfold thickness).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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A thorough understanding of the relationship between SM and obesity is important for the development of appropriate approaches to consider SM in clinical settings and in epidemiologic research when assessing child and adolescent obesity. Our findings of a reverse association between SM and fatness in boys add new insights into this issue and provide additional evidence for the influence of SM on fatness. The current evidence linking fatness and maturational events (eg, menarche) does not confirm the direction of causation, which remains controversial. On balance, although the mechanisms of puberty remain poorly understood,37 a growing literature seems to suggest a complex bidirectional causal relationship between early onset of puberty and obesity in females. According to Frisch’s well-known "critical weight (fat) hypothesis" developed in the 1970s, a certain amount or percentage of body fat is needed for the onset of menarche, ie, heavier girls mature earlier.7,8 It is hypothesized that subcutaneous fat tissue acts as a secondary hormonal gland and adipose tissue influences the synthesis and release of hormones (eg, estrogen), and thus promotes the onset of menarche.7,8,20 On the other hand, the critical weight hypothesis has been questioned and criticized by many others with accumulating contradictory evidence.5,9,18,19,21–23 Increasing evidence suggests that maturational timing affects body composition, at least, it has a greater long-term effect on fatness than the influence of fatness on the timing of SM.9–12,17 Some longitudinal studies suggest that earlier maturing girls have greater rates of increase in body weight and higher percentage of body fat and BMI than later maturing girls of the same age.10,12,17 This is particularly attributable to hormonal changes (eg, estrogen levels) associated with SM, which promotes the development of adipose tissue. Studies, predominantly for females, show that numerous factors such as genetic predisposition, diet, nutritional status, socioeconomic conditions, exercise, general health and well-being, and climate acting in combination influence SM.26,31,39,40 It is possible that some of these factors are the common causes of early onset of SM and obesity.
The gender difference we observed in the association between SM and obesity is likely attributable to the gender differences in biological development. The growth spurt in girls begins and ends earlier than in boys. During preadolescence, the proportions of adipose tissue and lean body mass in boys and girls are similar with body fat counts of 
15% and 19% muscle. In contrast, during adolescence, on average girls have relative greater increase in fat than fat-free mass, whereas boys gain more fat-free mass than fat mass. As a result, female adults have 22% body fat compared with an average of 15% in males; boys gain twice as much lean body mass as girls.31 We suspect that early onset of SM affects obesity partly because of its differential influence on growth in height and weight in boys and girls, whereas growth in height is a more important intermediate. For example, in boys, compared with average and late maturers, early maturers may utilize more energy and nutrients for growth in height while leaving less excess energy for the development of adipose tissue. We found that early-maturing boys were significantly taller, although their body weight was not significantly different from nonearly maturers. For girls, when height was adjusted, the association between early SM and obesity became insignificant in our study, although Adair and Gordon-Larsen4 reported early SM (based on menarcheal age) remained a significant risk factor even when height was adjusted for.
Aside from the possible biological mechanisms, it is also of interest for future studies to examine how behavioral, social, and environmental factors may contribute to the gender differences. In wealthy societies such as the United States, social norms and expectations toward body weight are different for females and males; for example, thinness is viewed as attractive for females, whereas for males, bigness and muscularness are desirable.37,41 This contributes to the gender differences in adolescents’ body image, eating behavior, and exercise patterns as suggested by the US Youth Risk Behavior Surveys.42,43 Studies from the development, psychology, and sociology literature suggest that pubertal development affects adolescents’ emotional and social problems such as depression, anxiety, and risky behaviors, and there are gender differences.44–46 It is possible that the interactions between biological maturation and social environmental factors play a role in the association between SM and obesity.
It has been of great interest to explain the ethnical disparities in obesity prevalence in the United States. Our findings that a large component of the ethnic differences (if not all) in fatness and obesity was explained by differences in SM provide some useful insights. For example, in girls, after controlling for SM stages, none of the ethnic differences in BMI, triceps skinfold, and sum of skinfolds remained statistically significant. Race/ethnicity was not a significant risk factor for overweight or obesity when early SM and other covariates such as diet and physical activity were adjusted for in the models. Our results are consistent with findings from the National Heart, Lung, and Blood Institute Growth and Health Study.15 Studying a cohort of 2799 9- to 10-year-old American white and black girls, Morrison et al15 found that after adjusting for maturation stage, the racial difference in BMI and the sum of skinfold thickness measurements became insignificant although on average black girls were fatter than white girls. A unique strength of the present study is that we were able to adjust for potential confounders such as diet and physical activity, which can help reduce potential bias.
Worth noting, we found that Mexican American boys remained at a higher risk of being obese than other race/ethnic groups even after controlling for SM and other covariates, which deserves additional investigation. The fact that Mexican American girls were not at an increased risk than other girls controlling for SM and other covariates indicates that genetic predisposition probably is not the full explanation for the racial/ethnic difference. Some risk factors related to ethnicity (eg, social and behavioral factors) may have not been measured adequately in the NHANES III data (eg, only one 24-hour dietary recall was collected); as a result, we could not control for them adequately. Furthermore, we tested the influence of height, another possible explanation for the ethnic difference in boys—BMI was associated with height during childhood and adolescence, and Mexican Americans were shorter than other ethnic groups. Interestingly, when height was adjusted for, the ethnic difference became greater (new OR, 95% CI: 2.53 [1.42, 4.51] for obesity). In summary, ours and others’ findings show that racial differences in obesity are related to racial differences in SM.
This study has a few limitations. First, cross-sectional data were used, and as a result, causality cannot be proven. One should be cautious to make inference regarding causality based on the present study. Second, it will be desirable if more accurate assessment of the timing of SM were available. In the present study, early SM is defined as those who reached a certain Tanner stage earlier than the medina age for that stage. SM is a developmental process and consists of different stages. There are within individual variation (differential development from one stage to another) and between individual differences in the developmental process of SM.26 The use of data collected at 1 time point (cross-sectional data) could misclassify some individuals’ SM status. In addition, it might be possible that heavier girls could be more likely to be classified as being at higher breast stages. This potentially might inflate the association between early SM and obesity; however, the influence seems to be very small considering findings by others. The OR we observed and that reported by Adair and Gordon-Larsen4 were consistent (they used age at menarche to classify early onset of SM). Finally, BMI percentiles were used to classify overweight and obesity following the CDC guidelines.35 Although BMI is a good measure for overweight and obesity screening,33–36 one needs to be aware of its limitations as an indirect measure of adiposity,47 such as it cannot distinguish lean body mass and adipose tissue. We attempted to address this weakness by using additional measures of skinfold thickness to assess the association between SM and fatness.
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CONCLUSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Reprint requests to (Y.W.) Department of Human Nutrition, M/C 517, University of Illinois at Chicago, 1919 W Taylor St, Chicago, IL 60612. E-mail: youfwang{at}uic.edu
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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