Background
Puberty is a period characterized by a growth spurt and rapid development of secondary sexual characteristics (breast budding, pubic hair growth and menarche in girls). The first visible evidence of puberty in girls is marked by thelarche, as developed by Tanner stages [
1] . Altered timing of puberty has significant clinical implications in pediatrics for the treatment of individual children. However, much of data on timing of puberty in girls focused on the age of menarche, which is easier to measure and least affected by observation errors [
2] .
Globally, most of the studies on timing of puberty were conducted using clinical samples [
2‐
5]. However, large scale, population-based epidemiologic data on puberty development is very important, for both pediatricians in precocious puberty and researchers focusing on the timing of puberty [
6] . The secular trend to earlier pubertal development in children and adolescents has been reported by many researchers, which was commonly ascribed by the improvement of nutritional and general health conditions [
2,
6,
7] . Yet it is worth noting that, during recent decades, several investigators noted a halt or even reversal in this trend in different countries, including China [
6,
8‐
10] .
Age of pubertal development has a great impact on health conditions, and early puberty might translate into increased risk for adult-onset diabetes, breast cancer, and all-cause mortality [
7,
11,
12] . The relationship between childhood adiposity, as assessed by body mass index (BMI), and earlier onset of puberty in girls has been reported in multiple studies [
13‐
15] . Existing Chinese studies on the relationship between obesity and pubertal attainment in girls were limited by lack of multiple measures of puberty development and different criteria of grouping childhood adiposity [
6] . Many epidemiologic studies used self-assessment of pubertal maturation, given that individual assessments by clinicians are time-consuming and expensive. Although central fat, measured by waist circumference (WC) and the waist-height ratio (WHtR), raises the risk for metabolic and cardiovascular complications in adolescents, it has been rarely used as the indicator of childhood adiposity in most findings [
16] .
To bridge the gap, we conducted a national cross-sectional study in China, to explore the association between body weight (overweight/obesity and central obesity) and attainment of puberty (breast development, pubic hair growth, and menarche) in Chinese Han schoolgirls. And we also wanted to estimate the ages of pubertal milestones for girls with and without obesity.
Results
Table
1 shows the descriptive characteristics of the girls in our study. A total of 2996 female Han Chinese girls aged 8.00–19.99 years participated in this study. Among them, 47.36% (
n = 1419) of the girls came from urban, and 52.64% (
n = 1577) lived in rural. According to the cutoffs of Chinese sex-age-specific BMI reference recommended by WGOC, more than 85% of the female students (85.88%,
n = 2573) were normal weight, 8.68% (
n = 260) were overweight, and 5.44% (
n = 163) were obese. The proportion of central obese was 14.69% using 0.5 cutoffs of WHtR, and the estimate was similar to the reference of 90th WC percentiles. Table
1 also displays the distribution of Tanner Stage of breast development and pubic hair development. 2169 girls (72.40%) experienced menarche.
Table 1
Descriptive Characteristics of the Population by Demographics and Development
Place |
Urban | 1419 | 47.36 |
Rural | 1577 | 52.64 |
Weight Status |
Normal weight | 2573 | 85.88 |
Overweight | 260 | 8.68 |
Obese | 163 | 5.44 |
WHtR |
< 0.5 | 2556 | 85.31 |
≥ 0.5 | 440 | 14.69 |
WC |
< 90th | 2670 | 89.12 |
≥ 90th | 326 | 12.88 |
Breast Development |
B1 | 201 | 6.71 |
B2 | 311 | 10.38 |
B3 | 705 | 23.53 |
B4 | 829 | 27.67 |
B5 | 950 | 31.71 |
Pubic Hair Growth |
PH1 | 578 | 19.29 |
PH2 | 376 | 12.55 |
PH3 | 603 | 20.13 |
PH4 | 791 | 26.40 |
PH5 | 648 | 21.63 |
Menarcheal status |
Yes | 2169 | 72.40 |
No | 827 | 27.60 |
Table
2 displays the median age at Tanner B2 or greater through B5 or greater according to obese status and demographics. The median age was 10.03 years at B2, 11.38 years at B3, 13.39 years at B4 and 15.79 years at B5. We found that the median age of girls marked as central obesity by either WHtR or WC were earlier than of normal girls across all stages of breast development, and all the differences were statistically significant. Similarly, compared with overweight or obesity group, there was evidence of a trend of later median age in normal weight group across all stages. However, we did not find any significant difference in timing of puberty between overweight and obesity. Besides, the median ages of urban girls were earlier than those of rural girls in all stages except in B5 or greater (15.70 years [urban] versus 15.88 years [rural];
P = 0.094).
Table 2
Median Age at Tanner Stages for Breast Development by Demographics
Overall | 10.03 (9.80, 10.27) | – | 11.38(11.26,11.49) | – | 13.39(13.29,13.49) | – | 15.79(15.69,15.90) | – |
Place |
Urban | 10.19(9.91,10.46) | | 11.26(11.11,11.41) | | 13.25(13.11,13.39) | | 15.70(15.54,15.85) | |
Rural | 9.85(9.45,10.25) | 0.187 | 11.50(11.33,11.66) | 0.043 | 13.51(13.37,13.64) | 0.010 | 15.88(15.73,16.03) | 0.094 |
WHtR |
< 0.5 | 10.12(9.89,10.5) | | 11.43(11.31,11.55) | | 13.48(13.37,13.59) | | 15.90(15.79,16.02) | |
≥ 0.5 | 9.00(7.60,10.41) | 0.007 | 11.00(10.59,11.41) | 0.013 | 12.92(12.70,13.14) | < 0.001 | 15.22(14.92,15.51) | < 0.001 |
WC |
< 90th | 10.05(9.81,10.29) | | 11.41(11.29,11.53) | | 13.48(13.37,13.58) | | 15.92(15.80,16.03) | |
≥ 90th | 8.44(4.23,12.65) | 0.052 | 10.65(9.79,11.52) | 0.001 | 12.77(12.48,13.07) | < 0.001 | 15.00(14.68,15.31) | < 0.001 |
BMI |
Normal weight | 10.25(10.03,10.47) | | 11.54(11.42,11.66) | | 13.48(13.38,13.59) | | 15.86(15.75,15.97) | |
Overweight | 8.64(6.85,10.43) | < 0.001a | 10.37(9.71,11.03) | < 0.001a | 12.83(12.54,13.13) | < 0.001a | 15.40(14.96,15.83) | 0.019a |
Obese | 8.60(6.54,10.65) | 0.002b | 10.66(10.00,11.31) | 0.001b | 12.93(12.51,13.36) | 0.015b | 15.16(14.67,15.66) | 0.004b |
| | 0.975c | | 0.570c | | 0.686c | | 0.495c |
Table
3 demonstrates differences in median age at Tanner PH2 or greater through PH5 or greater according to obese status and demographics. The median age was 11.62 years at PH2, 12.70 years at PH3, 14.38 years at PH4 and 16.92 years at PH5. These age differences for central obese/normal group, urban/rural area, overweight/normal weight and obese/normal weight group were consistent across all stages of pubic hair development. Compared with the obese group, there was evidence for later median age in the overweight group for PH2 or greater (11.31 years [overweight] versus 10.57 years [obese],
P = 0.021) and PH3 or greater (12.49 years [overweight] versus 11.93 years [obese],
P = 0.031).
Table 3
Median Age at Tanner Stages for Pubic Hair Development by Demographics
Overall | 11.62(11.51,11.73) | – | 12.70(12.61,12.80) | – | 14.38(14.28,14.48) | – | 16.92(16.78,17.06) | – |
Place |
Urban | 11.53(11.38,11.68) | | 12.38(12.24,12.53) | | 13.98(13.84,14.12) | | 16.61(16.43,16.78) | |
Rural | 11.70(11.55,11.85) | 0.132 | 12.97(12.85,13.10) | < 0.001 | 14.71(14.57,14.86) | < 0.001 | 17.25(17.02,17.48) | < 0.001 |
WHtR |
< 0.5 | 11.68(11.56,11.79) | | 12.76(12.66,12.86) | | 14.48(14.38,14.60) | | 16.98(16.84,17.13) | |
≥ 0.5 | 11.25(10.91,11.60) | 0.008 | 12.30(12.00,12.60) | 0.001 | 13.82(13.57,14.08) | < 0.001 | 16.55(16.15,16.94) | 0.029 |
WC |
< 90th | 11.68(11.57,11.79) | | 12.77(12.67,12.87) | | 14.49(14.38,14.59) | | 16.98(16.84,17.13) | |
≥ 90th | 9.83(8.37,11.30) | < 0.001 | 11.52(10.84,12.20) | < 0.001 | 13.63(13.31,13.94) | < 0.001 | 16.49(16.05,16.92) | 0.028 |
BMI |
Normal weight | 11.76(11.64,11.87) | | 12.79(12.69,12.90) | | 14.48(14.37,14.59) | | 17.01(16.87,17.16) | |
Overweight | 11.31(10.96,11.66) | 0.021a | 12.49(12.16,12.82) | 0.086a | 13.71(13.37,14.04) | < 0.001a | 16.03(15.59,16.47) | < 0.001a |
Obese | 10.57(10.00,11.14) | < 0.001b | 11.93(11.54,12.31) | < 0.00b | 13.81(13.45,14.18) | 0.003b | 16.29(15.52,17.06) | 0.022b |
| | 0.021c | | 0.031c | | 0.631c | | 0.535c |
The median age at menarche was 12.36 years for Chinese Han girls. As illustrated in Table
4, there was evidence of a trend for earlier median age of onset in urban (vs. rural) area, central obese (vs. normal group) group, overweight (vs. normal weight) and obese (vs. normal weight) group. We did not observe any significant difference in median age between overweight and obese subgroups.
Table 4
Median Age at Menarche by Demographics
Overall | 12.36(12.27,12.45) | – |
Place |
Urban | 12.17(12.04,12.30) | |
Rural | 12.52(12.40,12.65) | < 0.001 |
WHtR |
< 0.5 | 12.47(12.38,12.57) | |
≥ 0.5 | 11.70(11.43,11.97) | < 0.001 |
WC |
< 90th | 12.44(12.35,12.54) | |
≥ 90th | 11.48(11.04,11.93) | < 0.001 |
BMI |
Normal weight | 12.51(12.42,12.61) | |
Overweight | 11.75(11.50,12.00) | < 0.001a |
Obese | 11.44(11.04,11.84) | < 0.001b |
| | 0.175c |
Discussion
This study examined the association between timing of puberty staging (breast development, pubic hair development, and menarche) and obesity (overweight/obesity and central obesity) with a national sample of Han schoolgirls using a cross-sectional design. The measurements on puberty staging and obesity from clinical examinations were detailed and objective. This study adds unique and valuable data in Asian girls because existing large studies have focused more on European, African American or Hispanic descent populations [
5,
15,
18,
19].
Our findings add to evidence of earlier puberty (PH2 and PH3) for obese compared with normal or overweight girls. Also, there was suggestive evidence of later puberty (PH4 and PH5) for obese compared with overweight girls, although the differences in timing of PH4 and PH5 between the subgroups were non-significant. However, the differences of breast development and menarche were not significant between overweight and obese subgroups.
Considering that the effect of estrogen on the linear growth in humans is biphasic, low dose promotes, but high dose suppresses the linear growth [
26], it was hypothesized that excessive aromatase activity in adipose tissue produces increased level of estrogen, eventually results in possible delayed puberty. We found that compared with overweight girls, obese girls started PH2 earlier and attained PH4 and PH5 later, which indicates that excessive estrogen production in obese girls may inhibit the puberty process (PH4 and PH5) for obese, but not overweight, girls. Consistent with previous study conducted among boys [
27], our findings suggest that there is also a nonlinear relationship between pubic hair development and body fat for girls, which provides valuable insight into the complex relationship between puberty timing, overweight and obesity.
Note that it’s difficult to compare the results directly with previous studies, because the weight status data based on BMI, in most of the studies, were not divided into normal weight, overweight and obese sub groups [
28,
29]. In a national survey, Ying et al. found that an elevated BMI was associated with significantly earlier attainment of breast and menarche [
6] .
In our study, girls with central obesity, measured by either WC or WHtR, achieved all stages of breast and pubic hair development earlier than girls without central obesity. In adolescents, as in adults, central fat increases the risk for metabolic syndrome (dyslipidemia and insulin resistance) [
30,
31]. WC and WHtR in children are better indicators of distribution of body fat than BMI [
32,
33], easily measurable WC may be useful to help to identify vulnerable children [
34] . Our findings suggest that WC and WHtR can also server as obesity indicators to identify girls at risk of early pubertal onset.
In the present study, urban girls reached menarche earlier than girls living in rural places (12.17 years vs. 12.52 years,
p < 0.001) possibly because urban residents were more likely than rural residents to have access to high-quality food [
6] . However, we did not find the age differences of B2 and PH2 between urban and rural girls, which implies that breast and pubic hair development may be less sensitive than menarche to nutrition status [
6] . Body size parameters, such as BMI and body fat distribution are strongly correlated with the age at menarche. In our study, the median age of menarche of central obese and overweight/obese girls was earlier than that of normal girls. Frisch et al. proposed a critical body weight and weight gain to trigger the onset of puberty [
35] . Childhood adiposity may be considered as one of the predictors for the early occurrence of menarche [
36] .
Strengths and limitations
This study has several strengths. First, the present study included the subjects from a multi-provincial school-based population, which allows us to investigate the associations at the national level. Second, we rated puberty by triple objective indicators, assessed by clinicians, which is rare in large scale epidemiological studies. In addition, all the examinations were performed by the same group of reproductive endocrinologists, which guaranteed the comparability of results from diverse sites. The main limitation is that the nature of cross-sectional study cannot determine the direction of causality between pubertal development and obesity, obesity can both cause and result from pubertal development. Despite that, our study can help generate hypotheses to be explored using longitudinal studies. Second, we did not measure hormonal indictors, including estrogen, sex hormone-binding globulin, luteinizing hormone and follicle-stimulating hormone, which may confound our results because hormone could influence both puberty timing and weight status [
37]. Third, we failed to collect the information of the parents’ pubertal development, especially maternal history of precocious puberty, which may influence the pubertal development of their offspring. Fourth, participants were not sampled with multistage probability technique, which lowered its representativeness to a certain extent. Last, we may overestimate median age at Tanner B2 or greater given than we did not included children aged 6–7 years.
Conclusion
In conclusion, childhood obesity, including overweight/obesity and central obesity, is associated with earlier attainment of puberty at almost every pubertal stage of breast, pubic hair and menarche among Chinese Han schoolgirls. Our data support the potential nonlinear relationship between time of puberty and body fat in girls, which suggests that more studies are needed to explore the biological mechanisms behind.
Acknowledgements
The authors thank site coordinators of the 6 provinces for their hard work. The authors also appreciate the cooperation of the students involved.
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