Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Nutrition and Health (including climate and ecological aspects)

Prepubertal BMI, pubertal growth patterns, and long-term BMI: Results from a longitudinal analysis in Chinese children and adolescents from 2005 to 2016

European Journal of Clinical Nutrition volume 76, pages 1432–1439 (2022)Cite this article

Subjects

Abstract

Objective

To assess the effects of prepubertal BMI on pubertal growth patterns, and the influence of prepubertal BMI and pubertal growth patterns on long-term BMI among Chinese children and adolescents.

Methods

A total of 9606 individuals aged between 7 and 18 years from longitudinal surveys in Zhongshan city of China from 2005 to 2016 were enrolled. Age at peak height velocity (APHV) and peak height velocity (PHV) were estimated using Super-Imposition by Translation and Rotation (SITAR) model. Associations between prepubertal BMI, APHV, PHV, and long-term overweight and obesity were assessed by linear regression and multinominal logistic regression. Scatter plots were elaborated to show the associations between prepubertal BMI and pubertal growth patterns according to prepubertal BMI categories.

Results

Prepubertal BMI Z-Score was positively correlated with long-term BMI Z-Score, and negatively correlated with APHV in both sexes. In addition, there was a negative association between prepubertal BMI Z-Score and PHV in boys. With 1-year decrease in APHV, risk of long-term underweight decreased by 92%, while overweight increased by 33% in boys. Corresponding risk of long-term underweight and overweight for girls decreased by 42% and increased by 20%, respectively.

Conclusion

High prepubertal BMI levels were associated with earlier APHV and lower PHV, and the early onset of pubertal development could increase the risks of long-term overweight and obesity at 17–18 years of age both in boys and girls. Such evidence emphasized the importance of reducing prepubertal obesity risks combined with appropriate pubertal development timing, including later APHV and higher PHV, so as to prevent the obesity and related cardiovascular diseases in adulthood.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Scatter plot and linear fit line of association between prepubertal BMI and long-term BMI status, stratified by sex.
Fig. 2: Association between prepubertal BMI and pubertal growth patterns.
Fig. 3: Scatter plots and Linear fit line of participants’ prepubertal BMI z score and age at peak height velocity and magnitude of peak height velocity, stratified by prepubertal BMI status (underweight, normal weight, overweight, and obesity).

Data availability

The data are available from the corresponding author on reasonable request.

Code availability

The computer code and data sets generated and/or analyzed in the present study are not publicly available due to the need to protect participants privacy but are available from the corresponding author on reasonable request.

References

  1. NCD Risk Factor Collaboration. Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128.9 million children, adolescents, and adults. Lancet. 2017;390:2627–42.

    Article  Google Scholar 

  2. Popkin BM, Corvalan C, Grummer-Strawn LM. Dynamics of the double burden of malnutrition and the changing nutrition reality. Lancet. 2020;395:65–74.

    Article  PubMed  Google Scholar 

  3. Ward ZJ, Long MW, Resch SC, Giles CM, Cradock AL, Gortmaker SL. Simulation of growth trajectories of childhood obesity into adulthood. N Engl J Med. 2017;377:2145–53.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Black RE, Victora CG, Walker SP, Bhutta ZA, Christian P, de Onis M, et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet. 2013;382:427–51.

    Article  PubMed  Google Scholar 

  5. Patton GC, Viner R. Pubertal transitions in health. Lancet. 2007;369:1130–9.

    Article  PubMed  Google Scholar 

  6. Viner RM, Ross D, Hardy R, Kuh D, Power C, Johnson A, et al. Life course epidemiology: recognising the importance of adolescence. J Epidemiol Community Health. 2015;69:719–20.

    Article  PubMed  Google Scholar 

  7. Li W, Liu Q, Deng X, Chen Y, Liu S, Story M. Association between obesity and puberty timing: a systematic review and meta-analysis. Int J Environ Res Public Health. 2017;14:1266.

    Article  PubMed Central  Google Scholar 

  8. Gavela-Perez T, Garces C, Navarro-Sanchez P, Lopez Villanueva L, Soriano-Guillen L. Earlier menarcheal age in Spanish girls is related with an increase in body mass index between pre-pubertal school age and adolescence. Pediatr Obes. 2015;10:410–5.

    Article  CAS  PubMed  Google Scholar 

  9. Wagner IV, Sabin MA, Pfaffle RW, Hiemisch A, Sergeyev E, Korner A, et al. Effects of obesity on human sexual development. Nat Rev Endocrinol. 2012;8:246–54.

    Article  CAS  PubMed  Google Scholar 

  10. Barcellos Gemelli I, Farias E, Souza O. Age at menarche and its association with excess weight and body fat percentage in girls in the southwestern region of the Brazilian Amazon. J Pediatr Adolesc Gynecol. 2016;29:482–8.

    Article  PubMed  Google Scholar 

  11. Aksglaede L, Juul A, Olsen L, Sørensen T. Age at puberty and the emerging obesity epidemic. PLoS ONE. 2009;4:e8450.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Mouritsen A, Aksglaede L, Soerensen K, Hagen C, Petersen J, Main K, et al. The pubertal transition in 179 healthy Danish children: associations between pubarche, adrenarche, gonadarche, and body composition. Eur J Endocrinol. 2013;168:129–36.

    Article  CAS  PubMed  Google Scholar 

  13. Denzer C, Weibel A, Muche R, Karges B, Sorgo W, Wabitsch M. Pubertal development in obese children and adolescents. Int J Obes. 2007;31:1509–19.

    Article  CAS  Google Scholar 

  14. Day FR, Elks CE, Murray A, Ong KK, Perry JR. Puberty timing associated with diabetes, cardiovascular disease and also diverse health outcomes in men and women: the UK Biobank study. Sci Rep. 2015;5:11208.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Wang Y. Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls. Pediatrics. 2002;110:903–10.

    Article  PubMed  Google Scholar 

  16. 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.

    Article  PubMed  Google Scholar 

  17. Song Y, Ma J, Wang HJ, Wang Z, Hu P, Zhang B, et al. Trends of age at menarche and association with body mass index in Chinese school-aged girls, 1985-2010. J Pediatr. 2014;165:1172–7.e1.

    Article  PubMed  Google Scholar 

  18. Song Y, Ma J, Li L, Dong B, Wang Z, Agardh A. Secular trends for age at spermarche among Chinese boys from 11 ethnic minorities, 1995-2010: a multiple cross-sectional study. BMJ Open. 2016;6:e010518.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Cooper R, Blell M, Hardy R, Black S, Pollard TM, Wadsworth ME, et al. Validity of age at menarche self-reported in adulthood. J Epidemiol Community Health. 2006;60:993–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Walker IV, Smith CR, Davies JH, Inskip HM, Baird J. Methods for determining pubertal status in research studies: literature review and opinions of experts and adolescents. J Dev Orig Health Dis. 2020;11:168–87.

    Article  CAS  PubMed  Google Scholar 

  21. Malina R, Choh A, Czerwinski S, Chumlea W. Validation of maturity offset in the fels longitudinal study. Pediatr Exerc Sci. 2016;28:439–55.

    Article  PubMed  Google Scholar 

  22. Carrascosa A, Yeste D, Moreno-Galdo A, Gussinye M, Ferrandez A, Clemente M, et al. Pubertal growth of 1,453 healthy children according to age at pubertal growth spurt onset. The Barcelona longitudinal growth study. An Pediatr. 2018;89:144–52.

    Article  Google Scholar 

  23. Gasser T, Sheehy A, Largo RH. Statistical characterization of the pubertal growth spurt. Ann Hum Biol. 2001;28:395–402.

    Article  CAS  PubMed  Google Scholar 

  24. Bygdell M, Kindblom JM, Celind J, Nethander M, Ohlsson C. Childhood BMI is inversely associated with pubertal timing in normal-weight but not overweight boys. Am J Clin Nutr. 2018;108:1259–63.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Chen LK, Wang G, Bennett WL, Ji Y, Pearson C, Radovick S, et al. Trajectory of body mass index from ages 2 to 7 years and age at peak height velocity in boys and girls. J Pediatr. 2021;230:221–9.e5.

    Article  PubMed  Google Scholar 

  26. Ahmed M, Ong K, Dunger D. Childhood obesity and the timing of puberty. Trends Endocrinol Metab. 2009;20:237–42.

    Article  CAS  PubMed  Google Scholar 

  27. Tzoulaki I, Sovio U, Pillas D, Hartikainen A, Pouta A, Laitinen J, et al. Relation of immediate postnatal growth with obesity and related metabolic risk factors in adulthood: the northern Finland birth cohort 1966 study. Am J Epidemiol. 2010;171:989–98.

    Article  PubMed  Google Scholar 

  28. Boeyer M, Middleton K, Duren D, Leary E. Estimating peak height velocity in individuals: a comparison of statistical methods. Ann Hum Biol. 2020;47:434–45.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Wang X, Dong B, Huang S, Ma Y, Zou Z, Ma J, et al. Body mass index trajectory and incident hypertension: results from a longitudinal cohort of Chinese children and adolescents, 2006-16. Am J Public Health. 2020;110:1689–95.

    Article  PubMed  Google Scholar 

  30. de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85:660–7.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Silva AB, Capingana DP, Magalhaes P, Goncalves MA, Molina MD, Rodrigues SL, et al. Cardiovascular risk factors in pre-pubertal schoolchildren in Angola. Cardiovasc J Afr. 2016;27:315–21.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Buyken AE, Karaolis-Danckert N, Remer T. Association of prepubertal body composition in healthy girls and boys with the timing of early and late pubertal markers. Am J Clin Nutr. 2009;89:221–30.

    Article  CAS  PubMed  Google Scholar 

  33. Cole TJ, Donaldson MD, Ben-Shlomo Y. SITAR-a useful instrument for growth curve analysis. Int J Epidemiol. 2010;39:1558–66.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Cole TJ, Kuh D, Johnson W, Ward KA, Howe LD, Adams JE, et al. Using Super-Imposition by Translation And Rotation (SITAR) to relate pubertal growth to bone health in later life: the Medical Research Council (MRC) National Survey of Health and Development. Int J Epidemiol. 2016;45:1125–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Simmonds M, Llewellyn A, Owen CG, Woolacott N. Predicting adult obesity from childhood obesity: a systematic review and meta-analysis. Obes Rev. 2016;17:95–107.

    Article  CAS  PubMed  Google Scholar 

  36. Starc G, Strel J. Tracking excess weight and obesity from childhood to young adulthood: a 12-year prospective cohort study in Slovenia. Public Health Nutr. 2011;14:49–55.

    Article  PubMed  Google Scholar 

  37. Fonseca M, Oliveira A, Azevedo I, Nunes J, Santos A. Association of pubertal development with adiposity and cardiometabolic health in girls and boys-findings from the generation XXI birth cohort. J Adolesc Health. 2019;65:558–63.

    Article  PubMed  Google Scholar 

  38. Sandhu J, Ben-Shlomo Y, Cole TJ, Holly J, Davey Smith G. The impact of childhood body mass index on timing of puberty, adult stature and obesity: a follow-up study based on adolescent anthropometry recorded at Christ’s Hospital (1936-64). Int J Obes. 2006;30:14–22.

    Article  CAS  Google Scholar 

  39. He Q, Karlberg J. Bmi in childhood and its association with height gain, timing of puberty, and final height. Pediatr Res. 2001;49:244–51.

    Article  CAS  PubMed  Google Scholar 

  40. Fan H, Lee Y, Hsieh R, Yang C, Chen Y. Body mass index growth trajectories, early pubertal maturation, and short stature. Pediatr Res. 2020;88:117–24.

    Article  PubMed  Google Scholar 

  41. Biro FM, Khoury P, Morrison JA. Influence of obesity on timing of puberty. Int J Androl. 2006;29:272–7.

    Article  PubMed  Google Scholar 

  42. Bygdell M, Kindblom JM, Jansson JO, Ohlsson C. Revisiting the critical weight hypothesis for regulation of pubertal timing in boys. Am J Clin Nutr. 2020;113:123–8.

    Article  PubMed Central  Google Scholar 

  43. Boyne MS, Thame M, Osmond C, Fraser RA, Gabay L, Taylor-Bryan C, et al. The effect of earlier puberty on cardiometabolic risk factors in Afro-Caribbean children. J Pediatr Endocrinol Metab. 2014;27:453–60.

    Article  CAS  PubMed  Google Scholar 

  44. Widen E, Silventoinen K, Sovio U, Ripatti S, Cousminer DL, Hartikainen AL, et al. Pubertal timing and growth influences cardiometabolic risk factors in adult males and females. Diabetes Care. 2012;35:850–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Reinehr T, Roth CL. Is there a causal relationship between obesity and puberty? Lancet Child Adolesc Health. 2019;3:44–54.

    Article  PubMed  Google Scholar 

  46. Clayton PE, Trueman JA. Leptin and puberty. Arch Dis Child. 2000;83:1–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Mayes JS, Watson GH. Direct effects of sex steroid hormones on adipose tissues and obesity. Obes Rev. 2004;5:197–216.

    Article  CAS  PubMed  Google Scholar 

  48. Prentice P, Viner R. Pubertal timing and adult obesity and cardiometabolic risk in women and men: a systematic review and meta-analysis. Int J Obes. 2013;37:1036–43.

    Article  CAS  Google Scholar 

  49. Silventoinen K, Haukka J, Dunkel L, Tynelius P, Rasmussen F. Genetics of pubertal timing and its associations with relative weight in childhood and adult height: the Swedish Young Male Twins Study. Pediatrics. 2008;121:e885–91.

    Article  PubMed  Google Scholar 

  50. Yoshii K, Isojima T, Piedvache A, Morisaki N, Tanaka T, Nagata S. Reduced pubertal growth in children with obesity regardless of pubertal timing. Endocr J. 2020;67:477–84.

    Article  PubMed  Google Scholar 

  51. Oh CM, Oh IH, Choi KS, Choe BK, Yoon TY, Choi JM. Relationship between body mass index and early menarche of adolescent girls in Seoul. J Prev Med Public Health. 2012;45:227–34.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Kindblom JM, Lorentzon M, Norjavaara E, Lonn L, Brandberg J, Angelhed JE, et al. Pubertal timing is an independent predictor of central adiposity in young adult males: the Gothenburg osteoporosis and obesity determinants study. Diabetes 2006;55:3047–52.

    Article  CAS  PubMed  Google Scholar 

  53. Rogol A, Clark P, Roemmich J. Growth and pubertal development in children and adolescents: effects of diet and physical activity. Am J Clin Nutr. 2000;72:521S–8S.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the support from all the team members and the participating students, teachers, parents and local education and health staff in the programs.

Funding

The present study was supported by the National Natural Science Foundation (Grant 81673192 to JM; 82103865 to YD), and Beijing Natural Science Foundation (No. 7222244 to YD), as well as the China Postdoctoral Science Foundation (BX20200019 and 2020M680266 to YD).

Author information

Author notes

  1. These authors contributed equally: Yanhui Li, Di Gao, Jieyu Liu

  2. These authors jointly supervised this work: Yanhui Dong, Jun Ma.

Authors and Affiliations

  1. Institute of Child and Adolescent Health, School of Public Health, Peking University, 100191, Beijing, China

    Yanhui Li, Di Gao, Jieyu Liu, Zhaogeng Yang, Bo Wen, Li Chen, Manman Chen, Ying Ma, Tao Ma, Bin Dong, Yi Song, Yanhui Dong & Jun Ma

  2. National Health Commission Key Laboratory of Reproductive Health, 100191, Beijing, China

    Yanhui Li, Di Gao, Jieyu Liu, Zhaogeng Yang, Bo Wen, Li Chen, Manman Chen, Ying Ma, Tao Ma, Bin Dong, Yi Song, Yanhui Dong & Jun Ma

  3. Zhongshan Health Care Centers for Primary and Secondary School, 528403, Zhongshan, China

    Sizhe Huang

Authors
  1. Yanhui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Di Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jieyu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhaogeng Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bo Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Li Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Manman Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ying Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tao Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Bin Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yi Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Sizhe Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Yanhui Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jun Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YL, DG, and JL conceptualized and designed the study, completed the statistical analyses, drafted the initial paper, and reviewed and revised the paper; YD and JM contributed to the conceptualization and design of the study, supervised the data collection, the statistical analyses and initial drafting of the paper, and reviewed and revised the paper; BD, YS, and SH assisted with the statistical analyses and critically reviewed and revised the paper; ZY, BW, LC, MC, YM, and TM assisted with the data processing, statistical analyses, and the interpretation of the data. All authors approved the final paper as submitted and agree to be accountable for all aspects of the work.

Corresponding authors

Correspondence to Yanhui Dong or Jun Ma.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval and consent to participate

This study was conducted according to the guidelines laid down in the Declaration of Helsinki and all procedures involving students were approved by the Medical Research Ethics Committee of the Peking University Health Science Center (IRB00001052-20011). All participants and their parents signed informed consents voluntarily.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Gao, D., Liu, J. et al. Prepubertal BMI, pubertal growth patterns, and long-term BMI: Results from a longitudinal analysis in Chinese children and adolescents from 2005 to 2016. Eur J Clin Nutr 76, 1432–1439 (2022). https://doi.org/10.1038/s41430-022-01133-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41430-022-01133-2

Search

Advanced search

Quick links