Predicting Pubertal Development by Infantile and Childhood Height, BMI, and Adiposity Rebound
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nature publishing group Clinical Investigation Articles Predicting pubertal development by infantile and childhood height, BMI, and adiposity rebound Alina German1, Michael Shmoish2 and Ze’ev Hochberg3 BACKGROUND: Despite substantial heritability in puber- in these late maturing children is U-shaped (6,7). During the tal development, children differ in maturational tempo. transition from childhood to juvenility, which usually occurs Hypotheses: (i) puberty and its duration are influenced by early when children are aged about 6 y, the BMI rebounds immedi- changes in height and adiposity. (ii) Adiposity rebound (AR) is a ately after it reaches its nadir—the so-called adiposity rebound marker for pubertal tempo. (AR) (8,9). A young age and a high BMI at the age of rebound METHODS: We utilized published prospective data from 659 predicts a high BMI in early adulthood, and it has been sug- girls and 706 boys of the Study of Early Child Care and Youth gested that the occurrence of a high BMI at 3 y of age leads to Development. We investigated the age of pubarche-thelarche- a rebound at a younger age (10). gonadarche -menarche as a function of early height, BMI, and Since height and BMI at certain critical ages can predict AR. the timing and duration of puberty, the working hypotheses RESULTS: In girls, height standard deviation scores correlated of this investigation are (i) the onset of puberty, menarche, negatively with thelarche and pubarche from 15 mo of age and pubertal progression and duration are influenced by early and with menarche from 54 mo. BMI correlated negatively changes in height and adiposity and (ii) the age of occurrence with thelarche from 36 mo of age and menarche from 54 mo. of AR is an important marker of maturational tempo. Hence, In boys, age at gonadarche correlated negatively with height the purpose of this investigation was to examine the height from 36 mo of age. An AR was detected in 47% of girls and and BMI at different ages as they may predict pubertal timing 55% of boys, who became heavier and had earlier and faster and duration. To this end, we examined pubertal variability by puberty than those with no AR. assessing the effects of height, BMI, and AR at specific ages on CONCLUSION: The onset and tempo of puberty are influ- the timing and duration of puberty. For this purpose, we uti- enced by a two-hit program. The first is exerted during the lized the anthropological measurements and pubertal staging infancy–childhood transition (ICT; 6–12 mo) and includes data from American children of families that were recruited height, as an early predictor of maturational tempo. The sec- at 1 y of age in 1991 and followed up prospectively until 15.5 ond hit occurs at the childhood–juvenility transition (5–7 y) y of age for the National Institutes of Health (NICHD) Study and is based on adiposity and its rebound. of Early Child Care and Youth Development (SECCYD) (11). RESULTS he physiological variation in the age at the onset of puberty Pubertal development in boys and girls were assessed by Tcan be 4–5 y in normal children whose life conditions are clinical investigators of the SECCYD study and compared comparable and greater in children whose life conditions vary with the progress in the subjects’ BMI. In girls, thelarche (1). Despite substantial heritability in pubertal development occurred at 9.8 ± 0.7 y, pubarche occurred at 10.3 ± 0.7 y, and (2), children differ in their maturational tempos (3), and this menarche occurred at 12.3 ± 1.2 y (Table 1). In boys, gona- difference generates plasticity in their phenotypic trajectories darche occurred at 10.3 ± 0.5 y and pubarche occurred at so that they can adapt to their specific environment (4,5). The 11.4 ± 0.7 y. influence of socioeconomic status, diet, exercise, prepubertal fat and body weight, chronic illness, and stress on the age of Girls the onset of puberty is well documented (1). The influence of Figure 1 displays the relationships between thelarche, men- nutritional cues on the age at the onset of puberty are distinctly arche, and pubarche age, and the length/height standard devia- temporal: they tend to cause (i) early maturity in children whose tion scores (SDS) in the girls also shows the strengths of these average body mass in early life is either lower or higher than correlations as a function of age to pubertal onset. The length/ average and (ii) late maturity in children whose weight gain height SDS correlated negatively and significantly with thelar- during childhood is low (1). As a result, the pattern of growth che age from 15 mo of age (P < 0.0001; Figure 1a), menarche 1Pediatric Department, Bnai-Zion Medical Center and Clalit HMO, Haifa, Israel; 2Bioinformatics Knowledge Unit, The Lokey Center, Technion – Israel Institute of Technology, Haifa, Israel; 3The Ruth and Bruce Rappaport Faculty of Medicine, Technion – Israel Institute of Technology, Haifa, Israel. Correspondence: Alina German ([email protected]) Received 23 November 2014; accepted 2 April 2015; advance online publication 26 August 2015. doi:10.1038/pr.2015.129 Copyright © 2015 International Pediatric Research Foundation, Inc. Volume 78 | Number 4 | October 2015 Pediatric Research 445 Articles German et al. age from 54 mo of age (P = 0.014; Figure 1c), and pubarche age 0.016; Figure 2c), and pubarche from age 84 mo (P = 0.002; from 15 mo of age (P = 0.004; Figure 1e). In all instances, the Figure 2e). In all instances, the correlation strength increased correlation strength increased with age. with age. Pubertal progression or duration did not correlate Figure 2 displays the relationships between thelarche, men- with length/height or BMI at any age. arche, and pubarche age and BMI in the girls. BMI correlated An AR (Figure 3) was detected in 47% of girls (group 2; negatively and significantly with thelarche from 36 mo of age BMI SDS: 0.9 ± 0.9 at 7 y of age), and no AR was detected (P <0.0001; Figure 2a), menarche from 54 mo of age (P = in the remaining 53% (group 1); their 7 y of age BMI SDS was 0.0 ± 0.8, which is smaller than that of group 2 (P < 0.001). In Table 1. Tanner stages of pubertal development in 659 girls and 706 group 2 girls, thelarche and menarche occurred significantly boys for whom a full set of data was available for analysis earlier than its occurrence in group 1 girls (P = 0.030 and Girls Mean ± SD P = 0.017, respectively; Figure 4). No significant difference Thelarche age (years) 9.8 ± 0.7 was demonstrated between the groups in pubertal progression Pubarche age (years) 10.3 ± 0.7 (from B2 to menarche) 2.6 ± 0.1 vs. 2.5 ± 0.1 y and in the height at 15 y of age (164.3 ± 5.5 vs. 164.1 ± 6.5 cm). Menarche age (years) 12.3 ± 1.2 Breast full maturity age (years) 14.1 ± 0.8 Boys Pubic hair full maturity age (years) 14.1 ± 0.8 In boys, the age at gonadarche correlated negatively and Puberty progression (years) 2.5 ± 1.0 significantly with height from 36 mo of age (P < 0.001; Boys (n = 706) Mean ± SD Figure 5). The correlation strength did not changed with age Gonadarche age (years) 10.3 ± 0.6 and was smaller than that of the equivalent correlation strength in the girls. The age at pubarche correlated negatively and sig- Pubarche age (years) 11.4 ± 0.7 nificantly with height from 24 mo of age (P = 0.007). The corre- Genital full maturity age (years) 14.6 ± 0.6 lation strength did not change with age. The age at gonadarche Pubic hair full maturity age (years) 14.8 ± 0.6 and pubarche was not correlated with the BMI at any age. ac e 13 13 16 12 12 ears) 11 14 ears) ears) 11 10 12 B2 age (y P2 age (y 10 9 Menarche age (y 10 8 9 −3 −2 −10 123 −3 −2 −10 123 −3 −2 −10 123 Height SDS (15 m) Height SDS (54 m) Height SDS (15 m) bd f 0 10 .10 ) ) ) r r 10 r 20 .20 20 30 .30 30 40 .40 40 Correlation coefficient ( Correlation coefficient ( Correlation coefficient ( 50 50 .50 0204060 80 100 120 0204060 80 100 120 0204060 80 100 120 Age (mo) Age (mo) Age (mo) Figure 1. The relationships between thelarche, menarche, and pubarche age and the length/height standard deviation scores (SDS) in girls. (a) Thelarche age as a function of girls’ length at the age of 15 mo (r = −0.2; P = 0.0001), (c) menarche age as a function of girls’ height at the age of 54 mo (r = −0.16; P = 0.014), (e) pubarche age as a function of girls’ length at the age of 15 mo (r = −0.14; P = 0.004). (b, d, f) Correlation coefficients as a function of age for thelarche, menarche, and pubarche. The bold dots indicate the age at which the correlations became significant (P < 0.05). 446 Pediatric Research Volume 78 | Number 4 | October 2015 Copyright © 2015 International Pediatric Research Foundation, Inc. Programming for puberty Articles ace 12.5 15 12 11.5 ears) ears) ears) 13 11 10.5 P2 age (y B2 age (y 11 10 9.5 Menarche age (y 8.5 9 9 −20 2 4 −2 −1 0123 −3 −2 −1 0123 BMI SDS (36 mo) BMI SDS (54 mo) BMI SDS (84 mo) bdf −.10 00 .00 ) ) ) r r r −.15 10 .05 −.20 20 .10 −.25 30 .15 −.30 40 .20 Correlation coefficient ( .35 Correlation coefficient ( Correlation coefficient ( − −.40 50 .25 25 50 75 100 125 0 20 40 60 80 100 120 25 50 75 100 125 Age (mo) Age (mo) Age (mo) Figure 2.