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Weight Status in Young Girls and the Onset of Puberty

^a Pediatric Endocrinology
^b Child Health Evaluation and Research Unit
^f Child Behavioral Health, Department of Pediatrics
^d Center for Human Growth and Development, University of Michigan, Ann Arbor, Michigan
^c Data Coordinating Center, Boston University School of Public Health, Boston, Massachusetts
^e Center for Applied Studies in Education, University of Arkansas, Little Rock, Arkansas

	ABSTRACT

TOP ABSTRACT METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
OBJECTIVE. We sought to examine the association between weight status in early childhood and onset of puberty.

PATIENTS AND METHODS. The study included 354 girls from the National Institute of Child Health and Human Development Study of Early Child Care and Youth Development. Girls were followed longitudinally with height and weight measurements at 36 and 54 months and grades 1, 4, 5, and 6 and with assessment of pubertal stage by physical examination and maternal report in grades 4 through 6. The main outcome was the presence of early puberty, indexed as follows: (a) breast development at or more than Tanner stage 2 by physical examination at grade 4; (b) breast development at or more than Tanner stage 3 by physical examination at grade 5; (c) maternal report of breast development at or more than Tanner stage 3 at grade 5; and (d) maternal report of menarche having already occurred (yes versus no) at grade 6. Multiple logistic regression models predicting early versus late puberty were constructed by using the covariate BMI z score at 36 months, rate of change of BMI and accelerated BMI between 36 months and grade 1, race, maternal education, and maternal age of menarche.

RESULTS. BMI z score at 36 months, rate of change of BMI between 36 months and grade 1, an earlier age of maternal menarche, and nonwhite race were each consistently and positively associated with an earlier onset of puberty across the various measures of puberty.

CONCLUSIONS. Higher BMI z score in girls as young as 36 months of age and higher rate of change of BMI between 36 months old and grade 1, a period well before the onset of puberty, are associated with earlier puberty, which suggests that increasing rates of obesity in the United States may result in an earlier average age of onset of puberty for US girls.

Key Words: puberty • obesity • child • body weight • sexual maturation

Abbreviations: ITN—income-to-needs

A number of studies have evaluated the association between weight status and onset of puberty, because excess adiposity or body fatness is hypothesized to be a causal factor for early pubertal development in girls.¹ Cross-sectional studies have shown that pubertal girls have higher age- and gender-adjusted BMIs than their similarly aged prepubertal counterparts.^2,3 However, it is unclear whether increased body fatness precedes puberty or vice versa, given that puberty is a period associated with marked changes in body composition, including increases in fat mass and weight gain.⁴

The impact of weight status on puberty is a question of considerable importance, given that rates of obesity among children in the United States have doubled over the last 2 decades.^5,6 Studies suggest that girls are entering puberty at younger ages compared with 30 years ago,^7,8 and it has been hypothesized that the problem of childhood obesity is contributing to this secular trend.³

Longitudinal studies are, therefore, needed to evaluate the directionality of the relationship between weight and onset of puberty. One recently published longitudinal study demonstrated that girls with a higher percentage of body fat at 5 years old and girls with larger increases in percentage of body fat from 5 to 9 years of age were more likely to have pubertal development by age 9 years.⁹ These results offered evidence that increased weight status precedes and may, therefore, be causally linked to an earlier onset of puberty.⁹ However, given that the period between ages 5 and 9 years encompassed the onset of puberty, the directionality of the relationship between puberty and body fat may have been confounded, because studies have shown that onset of puberty is associated with increases in BMI.^2,10 We therefore sought to examine the association between weight status earlier than 5 years old and onset of puberty, using a longitudinal study design in a slightly larger sample of girls from diverse socioeconomic status drawn from 10 regions in the United States.

	METHODS

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The National Institute of Child Health and Human Development Study of Early Child Care and Youth Development is a longitudinal study of child behavior and development, particularly related to child care experiences.¹¹ Data from this study are available to qualified researchers by application. Parents and children were recruited through hospital visits to mothers shortly after the birth of a healthy singleton child in 1991 using a conditional random sampling plan. Details of the recruitment methods and sampling plan are available elsewhere.¹² Families lived in the areas of Little Rock, Arkansas; Irvine, California; Lawrence, Kansas; Boston, Massachusetts; Morganton, North Carolina; Philadelphia, Pennsylvania; Pittsburgh, Pennsylvania; Charlottesville, Virginia; Seattle, Washington; and Madison, Wisconsin. This study was approved by the institutional review boards of all of the pertinent institutions.

Anthropometric Data
The main predictor of interest was BMI before the onset of puberty. Height and weight were measured during laboratory visits at 36 months, 54 months, and grades 1, 4, 5, and 6 by trained research assistants.^13–15 BMI and BMI z score for each age were calculated using the 2000 Centers for Disease Control and Prevention growth charts.¹⁶ Girls were classified as "at risk for overweight" if age- and gender-specific BMI was 85th percentile and <95th percentile and "overweight" if BMI was 95th percentile.¹⁶

Puberty Measures
The outcome of interest was the presence of puberty, which we indexed as a dichotomous variable ("earlier puberty" versus "later puberty"). Measures of pubertal development were obtained at 3 annual laboratory visits occurring when girls were in grades 4 through 6, when girls were (mean ± SD) 9.6 ± 0.1, 10.6 ± 0.2, and 11.6 ± 0.1 year of age, respectively. Tanner staging at the laboratory visit physical examinations was performed by visual inspection by pediatric endocrinologists or nurse practitioners with experience in pubertal staging, using the methods of Herman-Giddens et al⁷ and others.¹⁷ Mothers reported their daughter's pubertal development at each of the 3 laboratory visits by selecting the drawing and description of the 5 stages of Tanner breast development that they felt was closest to their child's development.¹⁸ In addition, at each of the visits, mothers responded to the question, "Has [your daughter] had her first menstrual period?" (yes versus no).

We indexed the presence of early puberty through several different measurements of breast development, as well as the onset of menses, to enhance the validity of our findings. Early puberty was defined in the following 4 ways: (a) breast development at or more than Tanner stage 2 by physical examination at the grade 4 visit; (b) breast development at or more than Tanner stage 3 by physical examination at the grade 5 visit; (c) maternal report of breast development at or more than Tanner stage 3 at the grade 5 visit; and (d) maternal report of menarche having already occurred (yes versus no) at the grade 6 visit.

The first definition of puberty used in this study was breast development at or more than Tanner stage 2 by physical examination at the grade 4 visit, representing the textbook definition of onset of puberty in girls.¹⁹ This measure has been used to define puberty in previous studies^7,9 and provided a maximal sample size (n = 354). Because physical examination did not include breast palpation until 10.5 years of age in this study, excess fat could be mistaken for breast development in overweight girls, leading to misclassification of prepubertal girls as being in puberty.²⁰ Therefore, an alternate definition of puberty, breast development at or more than Tanner stage 3 by physical examination at the grade 5 visit was also assessed, which may be less prone to misclassification, but also resulted in a smaller sample size (n = 292). Some, but not all, studies²¹ have documented good agreement between physician- and subject-reported assessments of puberty, with a coefficient of 0.81²² or a correlation of r = 0.87²³ for female breast development. Therefore, maternal report of breast development at or more than Tanner stage 3 at the grade 5 visit (n = 328) was used to define earlier puberty. Cohen's for agreement of maternal report and physical examination for assessing at-or-more-than Tanner stage 3 development at grade 5 was 0.61 (95% confidence interval: 0.51–0.71). Finally, maternal report of menarche (yes versus no) at the grade 6 visit (n = 338) was used as a definition of earlier puberty. We chose to use the grade 6 maternal report of menses, because there was less missing information for the maternal report than for the grade 6 pubertal examination. In addition, assessment of Tanner staging in grade 6 would have represented a method that was similar to assessment of Tanner staging in grades 4 and 5, and we wished to use a different method for determining earlier and later onset of puberty.

Covariates
Mother-reported maternal age at menarche was included as a covariate given that later pubertal development in girls is associated with a maternal history of later pubertal development.²⁴ Studies have also shown that higher socioeconomic status is associated with earlier pubertal development in girls²⁴; therefore, the income-to-needs (ITN) ratio at 36 months old was included as a continuous variable. The ITN ratio represents total family income relative to the poverty line for a family of a particular size; families with an ITN ratio <1 are considered "poor." Maternal education, represented by the highest grade level of education completed by the mother, was a covariate, given that higher parental education in 1 previous study has been associated with earlier timing of puberty.²⁵ Finally, race was included as a covariate (dichotomized into the categories "white" and "nonwhite") given that black (compared with white) race is associated with earlier onset of puberty.^26,27

The initial sample in the study was composed of 1364 children (both boys and girls) and was representative of the demographics of the catchment areas from which the sample was recruited.¹¹ By grade 6, 1077 families remained in the study.²⁸ The sample for this analysis was restricted to girls with complete data for BMI at 36 months, 54 months, and grade 1; maternal age at menarche; and the pubertal outcome for each of the analyses. For the analysis for which the outcome was the presence of puberty based on physical examination Tanner staging at grade 4, complete data were available for 354 girls. The sample with complete data for BMI and puberty included in this analysis (n = 354) was compared with the sample with BMI but without puberty data (n = 92) by ² tests of association for categorical variables and t tests for continuous variables. Girls did not differ by race (P = .7), ITN ratio (P = .4), maternal education (P = .8), or BMI at grade 1 (P = .9).

Complete information on BMI, maternal age at menarche, and pubertal outcomes at later grades was available for a subset of the sample of 354 girls: 292 girls with a grade 5 physical examination, 328 girls with maternal report of Tanner stage 3 development in grade 5, and 338 girls with maternal report of menses in grade 6.

Analysis
All of the data analysis was performed by using SAS 9.1 (SAS Institute Inc, Cary, NC). Separate statistical analyses were conducted for each of the 4 different outcome measures of puberty. Bivariate statistics were performed to evaluate differences between girls who had earlier versus later puberty, and unadjusted analyses using logistic regression were performed to assess the association between BMI z score at each visit (36 months, 54 months, and grades, 1, 4, 5, and 6) and the odds of having earlier puberty.

The association between weight and early puberty could be related to the absolute BMI z score, the rate of change of BMI, or rapid increases in BMI early in childhood. Second-order polynomial trend scores were, therefore, created, using raw BMI scores rather than BMI z scores, because studies in similarly aged children suggest that raw BMI is superior to z scores for assessing changes in adiposity.²⁹ The first-order polynomial term assesses the rate (slope) of change on BMI between 36 months and grade 1. The second-order polynomial term, named accelerated BMI, assesses the rate of change in BMI growth between 36 months and grade 1. This term was calculated by subtracting the actual BMI at 54 months from the expected linear growth of BMI at 54 months. Expected linear growth of BMI at 54 months was determined by predicting BMI at 54 months based on the calculated slope of BMI change between 36 months and grade 1. Values close to 0 would indicate linear growth, and large values would indicate a nonlinear/quadratic pattern of increases in BMI with growth that is accelerated over this period, indicating a faster rate of gain in BMI between 54 months and grade 1.

The unadjusted associations between rate of change of BMI and accelerated BMI and the odds of having earlier puberty were evaluated. Because polynomial trend scores are orthogonal, multiple logistic regression models for predicting earlier puberty were then performed, including the covariates of BMI z score at 36 months old; rate of change of raw BMI between 36 months and grade 1; and the acceleration in change in BMI, race, maternal education, and maternal age at menarche. Because we did not find significant differences in the ITN ratio between girls with earlier and later puberty through our bivariate analyses, it was not included, to allow for the most parsimonious model. We evaluated for interactions between race and BMI z score, but these were not significant (data not shown).

	RESULTS

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Table 1 shows the demographic characteristics of the cohort overall and stratified by earlier and later puberty at the grade 4 visit. Most of the children were white, and of the nonwhite children (n = 63), 46 (73%) were black. Sixteen percent of the sample had an ITN ratio <1, indicating that they were living in poverty. In unadjusted bivariate analyses, earlier puberty was associated with nonwhite race, lower maternal education, earlier maternal age at menarche, and greater prevalence of child overweight and at risk for overweight. There were no significant differences in ITN ratio by puberty status.

	DISCUSSION

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A number of studies have suggested a causal link between excess body weight and an earlier timing of puberty. Frisch and McArthur¹ first hypothesized in 1974 that a "critical body weight" was necessary for the onset of puberty. Support for this hypothesis includes animal studies that have demonstrated that restricting weight gain delays the timing of puberty,³⁰ as well as a number of clinical studies that have found that pubertal girls have a higher BMI compared with their similarly aged prepubertal peers.^3,31

Longitudinal studies have investigated this issue further. Davison et al⁹ showed that higher BMI at 5 years and a greater increase in the percentage of body fat between ages 5 and 9 years were associated with earlier puberty in 180 white girls, offering evidence that weight status precedes pubertal timing. However, another longitudinal study of 211 white girls, the Fels Longitudinal Study, did not find an association between BMI during early childhood and age of menarche.³² That study only found differences in BMI between early and late maturing girls 4 to 6 years after puberty. Our study and the study by Davison et al⁹ had similar proportions of girls classified as at risk for overweight (16%) and overweight (13%), comparable to current national estimates of overweight in children,³³ with similar proportions of girls (50%) reaching Tanner stage 2 puberty at age 9. Although the rates of at risk for overweight and overweight in the population in the Fels Longitudinal Study were not reported, girls were from cohorts spanning the years 1929–1983, well before the increased prevalence of childhood overweight in the United States.⁵ Therefore, the lack of differences found in BMI between the early and late maturing groups in the Fels Longitudinal Study may be because of a low proportion of girls with excess weight in that population.

Strengths of our study include the longitudinal study design with BMI data from 36 months of age up to 12 years, the larger sample size, and the socioeconomic and geographic diversity of the sample, which allows for greater generalizability. Furthermore, we were able to adjust for other covariates known to influence the timing of puberty, including age of maternal menarche and race. We found that an earlier age of maternal menarche was associated with earlier puberty, which is consistent with studies in the literature.^24,34

In addition, although the number of nonwhite subjects in our sample was small, we did find that nonwhite children, of whom most were black, tended to have earlier puberty compared with white children, which has been reported previously in the literature.^2,7 We tested for but did not find significant interactions between race and BMI z score in our analysis, which is in contrast to the findings of Kaplowitz et al,³ who found a stronger relationship between BMI z score and puberty in white girls compared with black girls. It has been hypothesized that the pattern of earlier puberty seen in black girls compared with white girls could be related to the higher rates of at risk for overweight and overweight in black girls.⁹ The lack of a significant race x BMI interaction in our models would lend support for this hypothesis.

Similar to the study by Davison et al,⁹ our study did not use breast palpation for assessing puberty on physical examination at 9.5 years of age, although palpation was performed for girls starting at 10.5 years of age, which might lead to misclassification of pubertal status in overweight girls because of fat being confused with breast tissue.²⁰ However our study, as well as the study by Davison et al,²⁰ used multiple outcome measures of puberty to overcome this limitation. In addition to the standard clinical definition of puberty in girls (Tanner stage 2 puberty or greater breast development) we included the definition of Tanner stage 3 puberty or greater breast development by physical examination, which is a more conservative method for assessing puberty that is less likely prone to misclassification. Furthermore, we also used mother report of Tanner stage 3 puberty or greater breast development, as well as report of onset of menses by a mean age of 12 years, as pubertal measures. Given that mothers were asked to recall the onset of menses as a "yes" or "no" response, this method is likely less prone to recall bias than asking mothers a specific chronologic age at which onset of menses occurred.

Our study had several limitations. Fat mass was assessed with BMI, which is a surrogate measure of adiposity that correlates with fat-free mass, as well as total body fat, and does not account for differences in body fat distribution.³⁵ However, tests such as dual energy radiograph absorptiometry scans for body composition and computed tomography scans for fat distribution are likely not feasible in a large population-based study of girls. Furthermore, in this analysis, we did not evaluate for pubic hair development, which is a sign of increased adrenal androgen production or "adrenarche," a process that, on average, occurs at about the same time as pubertal breast development but is independent of the hypothalamic-pituitary-gonadal axis.³⁶ Finally, the girls in our study with "earlier" and "later" puberty cannot be considered to have either "precocious" or "delayed" puberty, because we evaluated puberty in a population of girls with normal growth and development starting at a mean age of 9 years.

	CONCLUSIONS

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Our finding that increased body fatness is associated with earlier pubertal development lends support for the hypothesis that increased rates of obesity among children in the United States may be contributing to a possible secular trend of early maturation in US girls.^3,27 Earlier onset of puberty in girls has been associated with a number of adverse outcomes, including psychiatric disorders and deficits in psychosocial functioning^37,38; earlier initiation of alcohol use, sexual intercourse and teenage pregnancy³⁹; and increased rates of adult obesity^40,41 and reproductive cancers.⁴² More studies are needed to identify the pathophysiologic mechanisms by which obesity leads to puberty and to determine whether interventions for weight control at an early age may slow or arrest the progression of pubertal onset to earlier ages in the population.

	ACKNOWLEDGMENTS

 
Dr Lee was supported by Pediatric Health Services Research Training Grant T32HD 07534–05 from the National Institute of Child Health and Human Development, National Institutes of Health. This project was supported by the American Heart Association Midwest Affiliate grant-in-aid 0455563Z (to Dr Lumeng).

	FOOTNOTES

 
Accepted Sep 15, 2006.

Address correspondence to Joyce M. Lee, MD, MPH, University of Michigan, 300 NIB, Room 6E05, Campus Box 0456, Ann Arbor, MI 48109-0456. E-mail: joyclee{at}umich.edu

This work was presented in part at the annual meeting of the Endocrine Society; June 24–27, 2006; Boston, MA.

The authors have indicated they have no financial relationships relevant to this article to disclose.

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TOP ABSTRACT METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 

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