Skip to main content
Top
Published in: BMC Pediatrics 1/2019

Open Access 01-12-2019 | Obesity | Research article

Puberty timing associated with obesity and central obesity in Chinese Han girls

Authors: Qiguo Lian, Yanyan Mao, Shan Luo, Shucheng Zhang, Xiaowen Tu, Xiayun Zuo, Chaohua Lou, Weijin Zhou

Published in: BMC Pediatrics | Issue 1/2019

Login to get access

Abstract

Background

There is growing scientific evidence supports a link between increased childhood adiposity and early onset of puberty in girls worldwide in recent decades. However, the data from Chinese girls remain ambiguous. The aims of this study were to estimate the puberty milestones and examine attainment of puberty associated with obesity and central obesity in Chinese Han schoolgirls.

Methods

The cross-sectional school-based study examined 2996 Han schoolgirls aged 9 to 19 years from 6 provinces in China. Trained clinicians assessed  the girls for height, weight, waist circumference, Tanner stages of breast and pubic hair development, and menarcheal status. We classified girls as normal weight, overweight, or obese based on BMI, and as normal weight or central obese based on the waist-height ratio, then estimated and compared median age at a given Tanner stage or greater by weight class using Probit models.

Results

The median age at menarche was 12.36 years. The median ages at breast stages(B) 2 through 5 were 10.03, 11.38, 13.39, and 15.79 years, respectively, and at pubic hair stages(PH) 2 through 5 were 11.62, 12.70, 14.38, and 16.92 years, respectively. Girls from urban areas experienced menarche, B3 and B4 stages, and PH3 through PH5 stages earlier. Girls with central obesity and overweight/obesity reached puberty earlier at almost every Tanner stage of breast and pubic hair than normal girls. Girls with obesity developed PH2 and PH3 earlier than their overweight peers. However, we did not find any significant differences between girls with overweight and obesity at all stages of breast development.

Conclusions

Childhood obesity, including both overweight/obesity and central obesity, is associated with earlier attainment of puberty in Chinese Han schoolgirls.
Literature
2.
go back to reference Ong KK, Ahmed ML, Dunger DB. Lessons from large population studies on timing and tempo of puberty (secular trends and relation to body size): the European trend. Mol Cell Endocrinol. 2006;254-255:8–12.PubMedCrossRef Ong KK, Ahmed ML, Dunger DB. Lessons from large population studies on timing and tempo of puberty (secular trends and relation to body size): the European trend. Mol Cell Endocrinol. 2006;254-255:8–12.PubMedCrossRef
3.
go back to reference Juul A, Teilmann G, Scheike T, Hertel NT, Holm K, Laursen EM, Main KM, Skakkebaek NE. Pubertal development in Danish children: comparison of recent European and US data. Int J Androl. 2006;29(1):247–55 discussion 286-290.PubMedCrossRef Juul A, Teilmann G, Scheike T, Hertel NT, Holm K, Laursen EM, Main KM, Skakkebaek NE. Pubertal development in Danish children: comparison of recent European and US data. Int J Androl. 2006;29(1):247–55 discussion 286-290.PubMedCrossRef
4.
go back to reference Aksglaede L, Sorensen K, Petersen JH, Skakkebaek NE, Juul A. Recent decline in age at breast development: the Copenhagen puberty study. Pediatrics. 2009;123(5):e932–9.PubMedCrossRef Aksglaede L, Sorensen K, Petersen JH, Skakkebaek NE, Juul A. Recent decline in age at breast development: the Copenhagen puberty study. Pediatrics. 2009;123(5):e932–9.PubMedCrossRef
5.
go back to reference Euling SY, Herman-Giddens ME, Lee PA, Selevan SG, Juul A, Sorensen TI, Dunkel L, Himes JH, Teilmann G, Swan SH. Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics. 2008;121 Suppl 3:S172–91.PubMedCrossRef Euling SY, Herman-Giddens ME, Lee PA, Selevan SG, Juul A, Sorensen TI, Dunkel L, Himes JH, Teilmann G, Swan SH. Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics. 2008;121 Suppl 3:S172–91.PubMedCrossRef
6.
go back to reference Sun Y, Tao FB, Su PY, Mai JC, Shi HJ, Han YT, Wang H, Lou XM, Han J, Liu J. National estimates of the pubertal milestones among urban and rural Chinese girls. J Adolesc Health. 2012;51(3):279–84.PubMedCrossRef Sun Y, Tao FB, Su PY, Mai JC, Shi HJ, Han YT, Wang H, Lou XM, Han J, Liu J. National estimates of the pubertal milestones among urban and rural Chinese girls. J Adolesc Health. 2012;51(3):279–84.PubMedCrossRef
7.
go back to reference Parent AS, Rasier G, Gerard A, Heger S, Roth C, Mastronardi C, Jung H, Ojeda SR, Bourguignon JP. Early onset of puberty: tracking genetic and environmental factors. Horm Res. 2005;64 Suppl 2:41–7.PubMed Parent AS, Rasier G, Gerard A, Heger S, Roth C, Mastronardi C, Jung H, Ojeda SR, Bourguignon JP. Early onset of puberty: tracking genetic and environmental factors. Horm Res. 2005;64 Suppl 2:41–7.PubMed
9.
go back to reference Atay Z, Turan S, Guran T, Furman A, Bereket A. Puberty and influencing factors in schoolgirls living in Istanbul: end of the secular trend? Pediatrics. 2011;128(1):e40–5.PubMedCrossRef Atay Z, Turan S, Guran T, Furman A, Bereket A. Puberty and influencing factors in schoolgirls living in Istanbul: end of the secular trend? Pediatrics. 2011;128(1):e40–5.PubMedCrossRef
10.
go back to reference Papadimitriou A. The evolution of the age at menarche from prehistorical to modern times. J Pediatr Adolesc Gynecol. 2016;29(6):527–30.PubMedCrossRef Papadimitriou A. The evolution of the age at menarche from prehistorical to modern times. J Pediatr Adolesc Gynecol. 2016;29(6):527–30.PubMedCrossRef
11.
go back to reference Lakshman R, Forouhi N, Luben R, Bingham S, Khaw K, Wareham N, Ong KK. Association between age at menarche and risk of diabetes in adults: results from the EPIC-Norfolk cohort study. Diabetologia. 2008;51(5):781–6.PubMedCrossRef Lakshman R, Forouhi N, Luben R, Bingham S, Khaw K, Wareham N, Ong KK. Association between age at menarche and risk of diabetes in adults: results from the EPIC-Norfolk cohort study. Diabetologia. 2008;51(5):781–6.PubMedCrossRef
12.
go back to reference Jacobsen BK, Heuch I, Kvale G. Association of low age at menarche with increased all-cause mortality: a 37-year follow-up of 61,319 Norwegian women. Am J Epidemiol. 2007;166(12):1431–7.PubMedCrossRef Jacobsen BK, Heuch I, Kvale G. Association of low age at menarche with increased all-cause mortality: a 37-year follow-up of 61,319 Norwegian women. Am J Epidemiol. 2007;166(12):1431–7.PubMedCrossRef
13.
go back to reference Biro FM, Greenspan LC, Galvez MP, Pinney SM, Teitelbaum S, Windham GC, Deardorff J, Herrick RL, Succop PA, Hiatt RA, et al. Onset of breast development in a longitudinal cohort. Pediatrics. 2013;132(6):1019–27.PubMedPubMedCentralCrossRef Biro FM, Greenspan LC, Galvez MP, Pinney SM, Teitelbaum S, Windham GC, Deardorff J, Herrick RL, Succop PA, Hiatt RA, et al. Onset of breast development in a longitudinal cohort. Pediatrics. 2013;132(6):1019–27.PubMedPubMedCentralCrossRef
14.
go back to reference Rosenfield RL, Lipton RB, Drum ML. Thelarche, pubarche, and menarche attainment in children with normal and elevated body mass index. Pediatrics. 2009;123(1):84–8.PubMedCrossRef Rosenfield RL, Lipton RB, Drum ML. Thelarche, pubarche, and menarche attainment in children with normal and elevated body mass index. Pediatrics. 2009;123(1):84–8.PubMedCrossRef
15.
go back to reference Kaplowitz PB, Slora EJ, Wasserman RC, Pedlow SE, Herman-Giddens ME. Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics. 2001;108(2):347–53.PubMedCrossRef Kaplowitz PB, Slora EJ, Wasserman RC, Pedlow SE, Herman-Giddens ME. Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics. 2001;108(2):347–53.PubMedCrossRef
16.
go back to reference Bacopoulou F, Efthymiou V, Landis G, Rentoumis A, Chrousos GP. Waist circumference, waist-to-hip ratio and waist-to-height ratio reference percentiles for abdominal obesity among Greek adolescents. BMC Pediatr. 2015;15(1):1–9.CrossRef Bacopoulou F, Efthymiou V, Landis G, Rentoumis A, Chrousos GP. Waist circumference, waist-to-hip ratio and waist-to-height ratio reference percentiles for abdominal obesity among Greek adolescents. BMC Pediatr. 2015;15(1):1–9.CrossRef
17.
go back to reference Song Y, Ma J, Agardh A, Lau PW, Hu P, Zhang B. Secular trends in age at menarche among Chinese girls from 24 ethnic minorities, 1985 to 2010. Glob Health Action. 2015;8:26929.PubMedCrossRef Song Y, Ma J, Agardh A, Lau PW, Hu P, Zhang B. Secular trends in age at menarche among Chinese girls from 24 ethnic minorities, 1985 to 2010. Glob Health Action. 2015;8:26929.PubMedCrossRef
18.
go back to reference Kaplowitz PB, Oberfield SE. Reexamination of the age limit for defining when puberty is precocious in girls in the United States: implications for evaluation and treatment. Drug and therapeutics and executive committees of the Lawson Wilkins pediatric Endocrine Society. Pediatrics. 1999;104(4 Pt 1):936–41.PubMedCrossRef Kaplowitz PB, Oberfield SE. Reexamination of the age limit for defining when puberty is precocious in girls in the United States: implications for evaluation and treatment. Drug and therapeutics and executive committees of the Lawson Wilkins pediatric Endocrine Society. Pediatrics. 1999;104(4 Pt 1):936–41.PubMedCrossRef
19.
go back to reference Chumlea WC, Schubert CM, Roche AF, Kulin HE, Lee PA, Himes JH, Sun SS. Age at menarche and racial comparisons in US girls. Pediatrics. 2003;111(1):110–3.PubMedCrossRef Chumlea WC, Schubert CM, Roche AF, Kulin HE, Lee PA, Himes JH, Sun SS. Age at menarche and racial comparisons in US girls. Pediatrics. 2003;111(1):110–3.PubMedCrossRef
20.
go back to reference Ji CY, Working Group on Obesity in C. Report on childhood obesity in China (1)--body mass index reference for screening overweight and obesity in Chinese school-age children. Biomed Environ Sci. 2005;18(6):390–400.PubMed Ji CY, Working Group on Obesity in C. Report on childhood obesity in China (1)--body mass index reference for screening overweight and obesity in Chinese school-age children. Biomed Environ Sci. 2005;18(6):390–400.PubMed
21.
go back to reference Yan W, Bingxian H, Hua Y, Jianghong D, Jun C, Dongliang G, Yujian Z, Ling L, Yanying G, Kaiti X, et al. Waist-to-height ratio is an accurate and easier index for evaluating obesity in children and adolescents. Obesity. 2007;15(3):748–52.CrossRef Yan W, Bingxian H, Hua Y, Jianghong D, Jun C, Dongliang G, Yujian Z, Ling L, Yanying G, Kaiti X, et al. Waist-to-height ratio is an accurate and easier index for evaluating obesity in children and adolescents. Obesity. 2007;15(3):748–52.CrossRef
22.
go back to reference Ma GS, Ji CY, Ma J, Mi J, Yt Sung R, Xiong F, Yan WL, Hu XQ, Li YP, Du SM, et al. Waist circumference reference values for screening cardiovascular risk factors in Chinese children and adolescents. Biomed Environ Sci. 2010;23(1):21–31.PubMedCrossRef Ma GS, Ji CY, Ma J, Mi J, Yt Sung R, Xiong F, Yan WL, Hu XQ, Li YP, Du SM, et al. Waist circumference reference values for screening cardiovascular risk factors in Chinese children and adolescents. Biomed Environ Sci. 2010;23(1):21–31.PubMedCrossRef
23.
go back to reference Xu J, Long JS. Confidence intervals for predicted outcomes in regression models for categorical outcomes. Stata J. 2005;5(4):537–59.CrossRef Xu J, Long JS. Confidence intervals for predicted outcomes in regression models for categorical outcomes. Stata J. 2005;5(4):537–59.CrossRef
24.
go back to reference Perneger TV. What’s wrong with Bonferroni adjustments. Br Med J. 1998;316(7139):1236–8.CrossRef Perneger TV. What’s wrong with Bonferroni adjustments. Br Med J. 1998;316(7139):1236–8.CrossRef
25.
go back to reference StataCorp. Stata Statistical Software: Release 14.1. College Station: StataCorp LP; 2015. StataCorp. Stata Statistical Software: Release 14.1. College Station: StataCorp LP; 2015.
26.
go back to reference Chagin AS, Savendahl L. Estrogens and growth: review. Pediatr Endocrinol Rev. 2007;4(4):329–34.PubMed Chagin AS, Savendahl L. Estrogens and growth: review. Pediatr Endocrinol Rev. 2007;4(4):329–34.PubMed
27.
go back to reference Lee JM, Wasserman R, Kaciroti N, Gebremariam A, Steffes J, Dowshen S, Harris D, Serwint J, Abney D, Smitherman L, et al. Timing of puberty in overweight versus obese boys. Pediatrics. 2016;137(2):e20150164.PubMedCrossRef Lee JM, Wasserman R, Kaciroti N, Gebremariam A, Steffes J, Dowshen S, Harris D, Serwint J, Abney D, Smitherman L, et al. Timing of puberty in overweight versus obese boys. Pediatrics. 2016;137(2):e20150164.PubMedCrossRef
28.
go back to reference Lee JM, Kaciroti N, Appugliese D, Corwyn RF, Bradley RH, Lumeng JC. Body mass index and timing of pubertal initiation in boys. Arch Pediatr Adolesc Med. 2010;164(2):139–44.PubMedPubMedCentralCrossRef Lee JM, Kaciroti N, Appugliese D, Corwyn RF, Bradley RH, Lumeng JC. Body mass index and timing of pubertal initiation in boys. Arch Pediatr Adolesc Med. 2010;164(2):139–44.PubMedPubMedCentralCrossRef
29.
go back to reference Crocker MK, Stern EA, Sedaka NM, Shomaker LB, Brady SM, Ali AH, Shawker TH, Hubbard VS, Yanovski JA. Sexual dimorphisms in the associations of BMI and body fat with indices of pubertal development in girls and boys. J Clin Endocrinol Metab. 2014;99(8):E1519–29.PubMedPubMedCentralCrossRef Crocker MK, Stern EA, Sedaka NM, Shomaker LB, Brady SM, Ali AH, Shawker TH, Hubbard VS, Yanovski JA. Sexual dimorphisms in the associations of BMI and body fat with indices of pubertal development in girls and boys. J Clin Endocrinol Metab. 2014;99(8):E1519–29.PubMedPubMedCentralCrossRef
30.
go back to reference Brambilla P, Manzoni P, Sironi S, Simone P, Del Maschio A, di Natale B, Chiumello G. Peripheral and abdominal adiposity in childhood obesity. Int J Obes Relat Metab Disord. 1994;18(12):795–800.PubMed Brambilla P, Manzoni P, Sironi S, Simone P, Del Maschio A, di Natale B, Chiumello G. Peripheral and abdominal adiposity in childhood obesity. Int J Obes Relat Metab Disord. 1994;18(12):795–800.PubMed
31.
go back to reference Caprio S, Hyman LD, McCarthy S, Lange R, Bronson M, Tamborlane WV. Fat distribution and cardiovascular risk factors in obese adolescent girls: importance of the intraabdominal fat depot. Am J Clin Nutr. 1996;64(1):12–7.PubMedCrossRef Caprio S, Hyman LD, McCarthy S, Lange R, Bronson M, Tamborlane WV. Fat distribution and cardiovascular risk factors in obese adolescent girls: importance of the intraabdominal fat depot. Am J Clin Nutr. 1996;64(1):12–7.PubMedCrossRef
32.
go back to reference Bacopoulou F, Efthymiou V, Landis G, Rentoumis A, Chrousos GP. Waist circumference, waist-to-hip ratio and waist-to-height ratio reference percentiles for abdominal obesity among Greek adolescents. BMC Pediatr. 2015;15:50.PubMedPubMedCentralCrossRef Bacopoulou F, Efthymiou V, Landis G, Rentoumis A, Chrousos GP. Waist circumference, waist-to-hip ratio and waist-to-height ratio reference percentiles for abdominal obesity among Greek adolescents. BMC Pediatr. 2015;15:50.PubMedPubMedCentralCrossRef
33.
34.
go back to reference Freedman DS, Serdula MK, Srinivasan SR, Berenson GS. Relation of circumferences and skinfold thicknesses to lipid and insulin concentrations in children and adolescents: the Bogalusa heart study. Am J Clin Nutr. 1999;69(2):308–17.PubMedCrossRef Freedman DS, Serdula MK, Srinivasan SR, Berenson GS. Relation of circumferences and skinfold thicknesses to lipid and insulin concentrations in children and adolescents: the Bogalusa heart study. Am J Clin Nutr. 1999;69(2):308–17.PubMedCrossRef
35.
go back to reference Frisch RE, Revelle R. Height and weight at menarche and a hypothesis of critical body weights and adolescent events. Science. 1970;169(3943):397–9.PubMedCrossRef Frisch RE, Revelle R. Height and weight at menarche and a hypothesis of critical body weights and adolescent events. Science. 1970;169(3943):397–9.PubMedCrossRef
37.
go back to reference Chen K, Corpus D, Zhong C, Rabii K, Klein K. Ethnicity and excess body weight impact on pubertal onset in girls: a longitudinal study of hormonal and bone maturation changes. J Pediatr Endocrinol. 2016;1(2):1007. Chen K, Corpus D, Zhong C, Rabii K, Klein K. Ethnicity and excess body weight impact on pubertal onset in girls: a longitudinal study of hormonal and bone maturation changes. J Pediatr Endocrinol. 2016;1(2):1007.
Metadata
Title
Puberty timing associated with obesity and central obesity in Chinese Han girls
Authors
Qiguo Lian
Yanyan Mao
Shan Luo
Shucheng Zhang
Xiaowen Tu
Xiayun Zuo
Chaohua Lou
Weijin Zhou
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Pediatrics / Issue 1/2019
Electronic ISSN: 1471-2431
DOI
https://doi.org/10.1186/s12887-018-1376-4

Other articles of this Issue 1/2019

BMC Pediatrics 1/2019 Go to the issue