Home Medicine Comparing adolescent self staging of pubertal development with hormone biomarkers
Article
Licensed
Unlicensed Requires Authentication

Comparing adolescent self staging of pubertal development with hormone biomarkers

  • Nana-Hawa Yayah Jones , Jane C. Khoury , Yingying Xu , Nicholas Newman , Heidi J. Kalkwarf , Joseph M. Braun , Bruce Lanphear , Aimin Chen , Kim M. Cecil , Susan R. Rose and Kimberly Yolton EMAIL logo
Published/Copyright: August 24, 2021

Abstract

Objectives

Physical examinations to characterize pubertal maturation may be unacceptable for children enrolled in research studies. Studies confirm the utility of pubertal self staging for research, but there has been limited comparison of self examination with hormone biomarkers. Our objective was to assess concordance of pubertal self staging with hormone biomarkers of puberty.

Methods

Participants were enrolled in the Health Outcomes and Measures of the Environment Study, a longitudinal pregnancy and birth cohort study. At age 12 years, 139 females and 112 males completed pubertal self staging including breast and pubic hair development in females and pubic hair development in males. No clinical physical examination was performed. Hormone concentrations were measured in 102 females and 96 males including serum dehydroepiandrosterone sulfate, luteinizing hormone, and follicle-stimulating hormone in all; estradiol in females; and testosterone in males.

Results

Estradiol was significantly associated with female breast stage, even when adjusted for BMI, with geometric least squares means (95%CI) of 13.2 (8.7, 20.2), 38.3 (29.9, 49.1), 59.4 (39.8, 88.6), and 81.2 (45.6, 144) pg/mL for breast stage 1–2, 3, 4, and 5, respectively. Testosterone was significantly associated with male pubic hair stage, with adjusted geometric least squares means (95%CI) of 37.6 (19.9, 71.1), 43.4 (27.7, 68.3), 126 (78.4, 203), 275 (146, 521), and 559 (237, 1319) ng/dL for pubic hair stage 1, 2, 3, 4, and 5, respectively.

Conclusions

Self assessed pubertal development was positively associated with hormonal biomarkers of puberty.


Corresponding author: Kimberly Yolton, PhD, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Avenue, MLC 7035 Cincinnati, OH 45229-3039, USA, Phone: +15136362815, E-mail:
Susan R. Rose and Kimberly Yolton Dual senior authors contributed equally.

Funding source: National Institute of Environmental Health Sciences doi.org/10.13039/100000066

Funding source: Environmental Protection Agency

Award Identifier / Grant number: P01ES011261

Award Identifier / Grant number: R01ES025214

Award Identifier / Grant number: R01ES027224

Acknowledgments

We are grateful to our participants for the time they have given to our study. All who have contributed significantly to this work have been acknowledged.

  1. Research funding: This work was supported by grants from the National Institute of Environmental Health Sciences and Environmental Protection Agency, P01ES011261, R01ES027224, R01ES025214.

  2. Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.

  3. Competing interests: Dr. Braun’s institution was financially compensated for his services as an expert witness for plaintiffs in litigation related to PFAS-contaminated drinking water; these funds were not paid to JMB directly. Dr. Braun received an honorarium for serving on an advisory board to Quest Diagnostics. All other authors declare no conflicts of interest.

  4. Informed consent: Informed consent was obtained from all individuals included in this study.

  5. Ethical approval: The local Institutional Review Board approved all study activities.

References

1. Kasper-Sonnenberg, M, Wittsiepe, J, Wald, K, Koch, HM, Wilhelm, M. Pre-pubertal exposure with phthalates and bisphenol A and pubertal development. PLoS One 2017;12:e0187922. https://doi.org/10.1371/journal.pone.0187922.Search in Google Scholar PubMed PubMed Central

2. Schoeters, G, Den Hond, E, Dhooge, W, Van Larebeke, N, Leijs, M. Endocrine disruptors and abnormalities of pubertal development. Basic Clin Pharmacol Toxicol 2008;102:168–75. https://doi.org/10.1111/j.1742-7843.2007.00180.x.Search in Google Scholar PubMed

3. Zawatski, W, Lee, MM. Male pubertal development: are endocrine-disrupting compounds shifting the norms. J Endocrinol 2013;218:R1–R12. https://doi.org/10.1530/joe-12-0449.Search in Google Scholar PubMed

4. Brooks-Gunn, J, Warren, MP. The psychological significance of secondary sexual characteristics in nine- to eleven-year-old girls. Child Development; 1988:1061–9 pp. https://doi.org/10.2307/1130272.Search in Google Scholar

5. Duren, DL, Nahhas, RW, Sherwood, RJ. Do secular trends in skeletal maturity Occur equally in both sexes? Clin Orthop Relat Res 2015;473:2559–67. https://doi.org/10.1007/s11999-015-4213-1.Search in Google Scholar PubMed PubMed Central

6. Herman-Giddens, ME, Slora, EJ, Wasserman, RC, Bourdony, CJ, Bhapkar, MV, Koch, GG, et al.. Secondary sexual characteristics and Menses in young girls seen in Office practice: a study from the pediatric research in Office settings Network. Pediatrics 1997;99:505–12. https://doi.org/10.1542/peds.99.4.505.Search in Google Scholar PubMed

7. Herman-Giddens, ME, Steffes, J, Harris, D, Slora, E, Hussey, M, Dowshen, SA, et al.. Secondary sexual characteristics in boys: data from the pediatric research in office settings network. Pediatrics 2012;130:e1058–e1068. https://doi.org/10.1542/peds.2011-3291.Search in Google Scholar PubMed

8. Himes, JH. Examining the evidence for recent secular changes in the timing of puberty in US children in Light of increases in the prevalence of obesity. Mol Cell Endocrinol 2006;254:13–21. https://doi.org/10.1016/j.mce.2006.04.013.Search in Google Scholar PubMed

9. 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;104:936–41. https://doi.org/10.1542/peds.104.4.936.Search in Google Scholar PubMed

10. 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;108:347–53. https://doi.org/10.1542/peds.108.2.347.Search in Google Scholar PubMed

11. Lee, JM, Wasserman, R, Kaciroti, N, Gebremariam, A, Steffes, J, Dowshen, S, et al.. Timing of puberty in Overweight versus obese boys. Pediatrics 2016;137:e20150164. https://doi.org/10.1542/peds.2015-0164.Search in Google Scholar PubMed

12. Ohlsson, C, Bygdell, M, Celind, J, Sonden, A, Tidblad, A, Savendahl, L, et al.. Secular trends in pubertal growth acceleration in Swedish boys Born from 1947 to 1996. JAMA Pediatrics 2019;173:860–5. https://doi.org/10.1001/jamapediatrics.2019.2315.Search in Google Scholar PubMed PubMed Central

13. Sørensen, K, Aksglaede, L, Petersen, JH, Juul, A. Recent changes in pubertal timing in Healthy Danish boys: associations with body mass index. J Clin Endocrinol Metab. 2010;95:263–70. https://doi.org/10.1210/jc.2009-1478.Search in Google Scholar PubMed

14. Tanner, JM. Growth at Adolescence, 2nd ed. Oxford: Blackwell Scientific Publications; 1962.Search in Google Scholar

15. Walker, I, Smith, C, Davies, J, Inskip, H, Baird, J. Methods for determining pubertal status in research studies: literature review and Opinions of experts and adolescents. Journal of Developmental Origins of Health and Disease 2020;11:168–87. https://doi.org/10.1017/s2040174419000254.Search in Google Scholar

16. Balzer, BW, Garden, FL, Amatoury, M, Luscombe, GM, Paxton, K, Hawke, CI, et al.. Self-rated tanner stage and subjective measures of puberty are associated with longitudinal gonadal hormone changes. J Pediatr Endocrinol Metab 2019;32:569–76. https://doi.org/10.1515/jpem-2019-0017.Search in Google Scholar PubMed

17. Chan, NP, Sung, RY, Kong, AP, Goggins, WB, So, HK, Nelson, EAS. Reliability of pubertal self-assessment in Hong Kong Chinese children. J Paediatr Child Health 2008;44:353–8. https://doi.org/10.1111/j.1440-1754.2008.01311.x.Search in Google Scholar PubMed

18. Chavarro, JE, Watkins, DJ, Afeiche, MC, Zhang, Z, Sanchez, BN, Cantonwine, D, et al.. Validity of self-assessed sexual maturation against physician assessments and hormone levels. J Pediatr 2017;186:172–8.e3. https://doi.org/10.1016/j.jpeds.2017.03.050.Search in Google Scholar PubMed PubMed Central

19. Jaruratanasirikul, S, Kreetapirom, P, Tassanakijpanich, N, Sriplung, H. Reliability of pubertal maturation self-assessment in a school-based survey. J Pediatr Endocrinol Metab 2015;28:367–74. https://doi.org/10.1515/jpem-2014-0053.Search in Google Scholar PubMed

20. Raman, A, Lustig, RH, Fitch, M, Fleming, SE. Accuracy of self-assessed tanner staging against hormonal assessment of sexual maturation in Overweight African-American children. J Pediatr Endocrinol Metab 2009;22:609–22. https://doi.org/10.1515/jpem.2009.22.7.609.Search in Google Scholar PubMed

21. Rapkin, AJ, Tsao, JC, Turk, N, Anderson, M, Zeltzer, LK. Relationships among self-rated tanner staging, hormones, and psychosocial factors in Healthy female adolescents. J Pediatr Adolesc Gynecol 2006;19:181–7. https://doi.org/10.1016/j.jpag.2006.02.004.Search in Google Scholar PubMed

22. Rasmussen, AR, Wohlfahrt-Veje, C, Tefre de Renzy-Martin, K, Hagen, CP, Tinggaard, J, Mouritsen, A, et al.. Validity of self-assessment of pubertal maturation. Pediatrics 2015;135:86–93. https://doi.org/10.1542/peds.2014-0793.Search in Google Scholar PubMed

23. Rollof, L, Elfving, M. Evaluation of self-assessment of pubertal maturation in boys and girls using drawings and orchidometer. J Pediatr Endocrinol Metab 2012;25:125–9. https://doi.org/10.1515/jpem.2011.440.Search in Google Scholar PubMed

24. Sun, Y, Tao, FB, Su, PY, Collaboration, CPR. Self-assessment of pubertal tanner stage by realistic Colour images in representative Chinese obese and non-obese children and adolescents. Acta Paediatr 2012;101:163–6. https://doi.org/10.1111/j.1651-2227.2011.02568.x.Search in Google Scholar PubMed

25. Wacharasindhu, S, Pri-Ngam, P, Kongchonrak, T. Self-assessment of sexual maturation in Thai children by tanner photograph. J Med Assoc Thailand 2002;85:308–19.Search in Google Scholar

26. Desmangles, J-C, Lappe, JM, Lipaczewski, G, Haynatzki, G. Accuracy of pubertal tanner staging self-reporting. J Pediatr Endocrinol Metab 2006;19:213–22. https://doi.org/10.1515/jpem.2006.19.3.213.Search in Google Scholar PubMed

27. Ernst, A, Lauridsen, L, Brix, N, Arah, OA, Olsen, J, Olsen, LH, et al.. Parental time to pregnancy, medically assisted reproduction and pubertal development in boys and girls. Hum Reprod 2019;34:724–32. https://doi.org/10.1093/humrep/dez008.Search in Google Scholar PubMed PubMed Central

28. Campisi, SC, Marchand, JD, Siddiqui, FJ, Islam, M, Bhutta, ZA, Palmert, MR. Can we rely on adolescents to self-assess puberty stage? A systematic review and meta-analysis. J Clin Endocrinol Metab. 2020;105:2846–56. https://doi.org/10.1210/clinem/dgaa135.Search in Google Scholar PubMed

29. Terry, MB, Goldberg, M, Schechter, S, Houghton, LC, White, ML, O’Toole, K, et al.. Comparison of clinical, maternal, and self pubertal assessments: implications for health studies. Pediatrics 2016;138:e20154571. https://doi.org/10.1542/peds.2015-4571.Search in Google Scholar PubMed PubMed Central

30. Oerter, K, Uriate, M, Rose, S, Barnes, K, Cutler, G. Gonadotropin secretory dynamics during puberty in normal girls and boys. J Clin Endocrinol Metab. 1990;71:1251–8. https://doi.org/10.1210/jcem-71-5-1251.Search in Google Scholar PubMed

31. Kletter, G, Padmanabhan, V, Brown, MB, Reiter, E, Sizonenko, P, Beitins, I. Serum bioactive gonadotropins during male puberty: a longitudinal study. J Clin Endocrinol Metab. 1993;76:432–8. https://doi.org/10.1210/jcem.76.2.8432787.Search in Google Scholar PubMed

32. Kasa-Vubu, JZ, Padmanabhan, V, Kletter, GB, Brown, MB, Reiter, EO, Sizonenko, PC, et al.. Serum bioactive luteinizing and follicle-stimulating hormone concentrations in girls increase during puberty. Pediatr Res 1993;34:829–33. https://doi.org/10.1203/00006450-199312000-00026.Search in Google Scholar PubMed

33. Shirtcliff, EA, Dahl, RE, Pollak, SD. Pubertal development: correspondence between hormonal and physical development. Child Dev 2009;80:327–37. https://doi.org/10.1111/j.1467-8624.2009.01263.x.Search in Google Scholar PubMed PubMed Central

34. Braun, JM, Buckley, JP, Cecil, KM, Chen, A, Kalkwarf, HJ, Lanphear, BP, et al.. Adolescent follow-up in the health outcomes and measures of the environment (HOME) study: cohort profile. BMJ Open 2020;10:e034838. https://doi.org/10.1136/bmjopen-2019-034838.Search in Google Scholar PubMed PubMed Central

35. Braun, JM, Kalloo, G, Chen, A, Dietrich, KN, Liddy-Hicks, S, Morgan, S, et al.. Cohort profile: the health outcomes and measures of the environment (HOME) study. Int J Epidemiol 2017;46:24. https://doi.org/10.1093/ije/dyw006.Search in Google Scholar PubMed PubMed Central

36. Landis, JR, Koch, GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159–74. https://doi.org/10.2307/2529310.Search in Google Scholar

37. Biro, FM, Khoury, P, Morrison, JA. Influence of obesity on timing of puberty. Int J Androl 2006;29:272–7. https://doi.org/10.1111/j.1365-2605.2005.00602.x.Search in Google Scholar PubMed

38. Brix, N, Ernst, A, Lauridsen, LL, Arah, OA, Nohr, EA, Olsen, J, et al.. Maternal pre-pregnancy obesity and timing of puberty in Sons and Daughters: a population-based cohort study. Int J Epidemiol 2019;48:1684–94. https://doi.org/10.1093/ije/dyz125.Search in Google Scholar PubMed PubMed Central

39. Turan, S, Bereket, A, Guran, T, Akcay, T, Papari-Zareei, M, Auchus, RJ. Puberty in a case with novel 17-hydroxylase mutation and the putative role of estrogen in development of pubic hair. Eur J Endocrinol 2009;160:325–30. https://doi.org/10.1530/eje-08-0632.Search in Google Scholar PubMed

40. Guran, T, Firat, I, Yildiz, F, Kaplan Bulut, I, Dogru, M, Bereket, A. Reference values for serum dehydroepiandrosterone-sulphate in Healthy children and adolescents with Emphasis on the age of adrenarche and pubarche. J Clin Endocrinol Metab 2015;82:712–8. https://doi.org/10.1111/cen.12612.Search in Google Scholar PubMed

41. Kretsch, N, Mendle, J, Cance, JD, Harden, KP. Peer group similarity in perceptions of pubertal timing. J Youth Adolesc 2016;45:1696–710. https://doi.org/10.1007/s10964-015-0275-3.Search in Google Scholar PubMed PubMed Central

42. Plant, TM. Neuroendocrine control of the onset of puberty. Front Neuroendocrinol 2015;38:73–88. https://doi.org/10.1016/j.yfrne.2015.04.002.Search in Google Scholar PubMed PubMed Central


Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/jpem-2021-0366).


Received: 2021-05-25
Accepted: 2021-08-06
Published Online: 2021-08-24
Published in Print: 2021-12-20

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. Review Article
  3. Calcitonin and complementary biomarkers in the diagnosis of hereditary medullary thyroid carcinoma in children and adolescents
  4. Original Articles
  5. Genotype and phenotypic spectrum of vitamin D dependent rickets type 1A: our experience and systematic review
  6. Questioning the adequacy of standardized vitamin D supplementation protocol in very low birth weight infants: a prospective cohort study
  7. Growth hormone replacement therapy: is it safe to use in children with asymptomatic pituitary lesions?
  8. Comparing adolescent self staging of pubertal development with hormone biomarkers
  9. Reverse circadian glucocorticoid treatment in prepubertal children with congenital adrenal hyperplasia
  10. The concordance between ultrasonographic stage of breast and Tanner stage of breast for overweight and obese girls: a school population-based study
  11. Cross-sectional analysis: clinical presentation of children with persistently low ALP levels
  12. The utility of continuous glucose monitoring systems in the management of children with persistent hypoglycaemia
  13. Long-term effect of conventional phosphate and calcitriol treatment on metabolic recovery and catch-up growth in children with PHEX mutation
  14. Role of magnetic resonance diffusion weighted imaging in diagnosis of diabetic nephropathy in children living with type 1 diabetes mellitus
  15. Investigation of quality of life in obese adolescents: the effect of psychiatric symptoms of obese adolescent and/or mother on quality of life
  16. Predictive value of WHO vs. IAP BMI charts for identification of metabolic risk in Indian children and adolescents
  17. Case Reports
  18. COVID-19 triggered encephalopathic crisis in a patient with glutaric aciduria type 1
  19. Aromatase deficiency in an Ontario Old Order Mennonite family
  20. A case of monogenic diabetes mellitus caused by a novel heterozygous RFX6 nonsense mutation in a 14-year-old girl
Downloaded on 19.12.2025 from https://www.degruyterbrill.com/document/doi/10.1515/jpem-2021-0366/html
Scroll to top button