Abstract
Objectives
In this study, we evaluated the concordance between the ultrasonographic stage of breast (US B) and Tanner stage of breast (TS B) for overweight and obese girls based on a school population study.
Methods
We conducted multistage, stratified cluster, and random-proportional sampling and ultimately included 221 girls (aged 6–10 years).
Results
This study revealed that the concordance was poor (accuracy=0.19 (95% confidence interval: 0.14, 0.25)) between US B and TS B among the 221 participants. When our subjects were stratified by weight, we observed a weak association between US B and TS B in the thin/normal weight group (r=0.34, p=0.001) but not in the overweight (r=0.097, p=0.38) or obese groups (r=–0.19, p=0.206), and as the body mass index (BMI) z-score increased, the overestimation ratio of TS B increased. US B manifested a positive correlation with breast bud diameter (BD) (r=0.885, p<0.001), follicle-stimulating hormone (r=0.235, p=0.009), and luteinizing hormone (r=0.192, p=0.037), but this was not the case with TS B.
Conclusions
As the BMI z-score increased, the correlation between the two methods declined, and the overestimation ratio of TS B increased. US B is an objective and quantitative method used to evaluate breast development, and whether BD might replace US B as a routine diagnostic method to evaluate breast development in clinical practice needs to be confirmed in larger-sample studies.
Funding source: National Science Foundation of China
Award Identifier / Grant number: 81872637, 81903341, 82173534
Funding source: Shanghai Professional and Technical Services Platform
Award Identifier / Grant number: 18DZ2294100
Funding source: Foundation of National Facility for Translational Medicine, Shanghai
Award Identifier / Grant number: TMSK-2020-124
Funding source: Key Subject Program for Clinical Nutrition from Shanghai Municipal Health Commission
Award Identifier / Grant number: 2019ZB0103
Funding source: Key discipline construction project of the three-year action Plan of Shanghai Public Health System
Award Identifier / Grant number: GWV-10.1-XK07
Funding source: Zhongshan City Social Welfare Science and Technology Research Project
Award Identifier / Grant number: 2019B1017
Acknowledgments
The authors would like to express our gratitude to the participants’ parents for their understanding and cooperation in this study.
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Research funding: This study was supported by National Science Foundation of China [81872637, 81903341, 82173534], and Shanghai Professional and Technical Services Platform [18DZ2294100], the Foundation of National Facility for Translational Medicine, Shanghai [TMSK-2020-124], Key Subject Program for Clinical Nutrition from Shanghai Municipal Health Commission [2019ZB0103], Key discipline construction project of the three-year action Plan of Shanghai Public Health System [GWV-10.1-XK07] and Zhongshan City Social Welfare Science and Technology Research Project (2019B1017).
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Author contributions: X.Y., S.F., C.L., and S.L. designed the study. S.F., C.L., S.L., T.Y., S.H., B.Z., and D.P. participated in the research’s investigation and coordination work, specimen and data collection. D.P., T.Y., and S.L. were responsible for data analysis. D.P., and S.L. drafted the main manuscript. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
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Competing interests: Authors declare no conflict of interest.
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Informed consent: Informed consent was obtained from all individuals included in this study.
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Ethical approval: The study was approved by local institutional review boards and all participants (or their legally guadians) provided written informed consent and was conducted according to the Declaration of Helsinki and the present study was registered in the Protocol Registration and Results System (ClinicalTrials.gov, NCT04113070).
References
1. Biro, FM, Greenspan, LC, Galvez, MP, Pinney, SM, Teitelbaum, S, Windham, GC, et al.. Onset of breast development in a longitudinal cohort. Pediatrics 2013;132:1019–27. https://doi.org/10.1542/peds.2012-3773.Search in Google Scholar
2. Chen, C, Zhang, Y, Sun, W, Chen, Y, Jiang, Y, Song, Y, et al.. Investigating the relationship between precocious puberty and obesity: a cross-sectional study in Shanghai, China. BMJ Open 2017;7: e014004. https://doi.org/10.1136/bmjopen-2016-014004.Search in Google Scholar
3. Lian, Q, Mao, Y, Luo, S, Zhang, S, Tu, X, Zuo, X, et al.. Puberty timing associated with obesity and central obesity in Chinese Han girls. BMC Pediatr 2019;19:1. https://doi.org/10.1186/s12887-018-1376-4.Search in Google Scholar
4. Eckert-Lind, C, Busch, AS, Petersen, JH, Biro, FM, Butler, G, Bräuner, EV, et al.. Worldwide secular trends in age at pubertal onset assessed by breast development among girls: a systematic review and meta-analysis. JAMA Pediatr 2020;174: e195881. https://doi.org/10.1001/jamapediatrics.2019.5881.Search in Google Scholar
5. Marshall, WA, Tanner, JM. Variations in pattern of pubertal changes in girls. Arch Dis Child 1969;44:291–303. https://doi.org/10.1136/adc.44.235.291.Search in Google Scholar
6. Fugl, L, Hagen, CP, Mieritz, MG, Tinggaard, J, Fallentin, E, Main, KM, et al.. Glandular breast tissue volume by magnetic resonance imaging in 100 healthy peripubertal girls: evaluation of clinical Tanner staging. Pediatr Res 2016;80:526–30. https://doi.org/10.1038/pr.2016.125.Search in Google Scholar
7. Yüce, Ö, Sevinç, D. Ultrasonographic assessment of pubertal breast development in obese children: compliance with the clinic. J Pediatr Endocrinol Metab 2018;31:137–41. https://doi.org/10.1515/jpem-2017-0243.Search in Google Scholar
8. Bruni, V, Dei, M, Deligeoroglou, E, Innocenti, P, Bassi, F. Breast development in adolescent girls. Adolesc Pediatr Gynecol 1990;3:201–5. https://doi.org/10.1016/s0932-8610(19)80037-3.Search in Google Scholar
9. Calcaterra, V, Sampaolo, P, Klersy, C, Larizza, D, Alfei, A, Brizzi, V, et al.. Utility of breast ultrasonography in the diagnostic work-up of precocious puberty and proposal of a prognostic index for identifying girls with rapidly progressive central precocious puberty. Ultrasound Obstet Gynecol 2009;33:85–91. https://doi.org/10.1002/uog.6271.Search in Google Scholar PubMed
10. Carlson, L, Flores Poccia, V, Sun, BZ, Mosley, B, Kirste, I, Rice, A, et al.. Early breast development in overweight girls: does estrogen made by adipose tissue play a role? Int J Obes 2019;43:1978–87. https://doi.org/10.1038/s41366-019-0446-5.Search in Google Scholar PubMed PubMed Central
11. Bruserud, IS, Roelants, M, Oehme, NHB, Madsen, A, Eide, GE, Bjerknes, R, et al.. References for ultrasound staging of breast maturation, Tanner breast staging, pubic hair, and menarche in Norwegian Girls. J Clin Endocrinol Metab 2020;105:1599–607. https://doi.org/10.1210/clinem/dgaa107.Search in Google Scholar PubMed PubMed Central
12. Liu, Y, Yu, T, Li, X, Pan, D, Lai, X, Chen, Y, et al.. Prevalence of precocious puberty among Chinese children: a school population-based study. Endocrine 2021;72:573–81. https://doi.org/10.1007/s12020-021-02630-3.Search in Google Scholar PubMed
13. Cole, TJ, Flegal, KM, Nicholls, D, Jackson, AA. Body mass index cut offs to define thinness in children and adolescents: international survey. BMJ 2007;28:335–194. https://doi.org/10.1136/bmj.39238.399444.55.Search in Google Scholar PubMed PubMed Central
14. Cole, TJ, Bellizzi, MC, Flegal, KM, Dietz, WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 2000;320:1240–3. https://doi.org/10.1136/bmj.320.7244.1240.Search in Google Scholar PubMed PubMed Central
15. World Health Organization. Growth Reference Data for Children From 5 to 19 Years, 2007. Geneva: WHO; 2007. Available from: http://www.who.int/growthref/en/.Search in Google Scholar
16. García, CJ, Espinoza, A, Dinamarca, V, Navarro, O, Daneman, A, García, H, et al.. Breast US in children and adolescents. Radiographics 2000;20:1605–12. https://doi.org/10.1148/radiographics.20.6.g00nv171605.Search in Google Scholar PubMed
17. Huen, KF, Leung, SS, Lau, JT, Cheung, AY, Leung, NK, Chiu, MC. Secular trend in the sexual maturation of southern Chinese girls. Acta Paediatr 1997;86:1121–4. https://doi.org/10.1111/j.1651-2227.1997.tb14820.x.Search in Google Scholar PubMed
18. Ma, HM, Du, ML, Luo, XP, Chen, SK, Liu, L, Chen, RM, et al.. Onset of breast and pubic hair development and menses in urban Chinese girls. Pediatrics 2009;124:e269–277. https://doi.org/10.1542/peds.2008-2638.Search in Google Scholar PubMed
19. Sun, Y, Tao, FB, Su, PY, Mai, JC, Shi, HJ, Han, YT, et al.. National estimates of the pubertal milestones among urban and rural Chinese girls. J Adolesc Health 2012;51:279–84. https://doi.org/10.1016/j.jadohealth.2011.12.019.Search in Google Scholar PubMed
20. Li, W, Liu, Q, Deng, X, Chen, Y, Yang, B, Huang, X, et al.. Association of prepubertal obesity with pubertal development in Chinese girls and boys: a longitudinal study. Am J Hum Biol 2018;30: e23195. https://doi.org/10.1002/ajhb.23195.Search in Google Scholar PubMed PubMed Central
21. 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 Publ Health 2017;14:1266. https://doi.org/10.3390/ijerph14101266.Search in Google Scholar PubMed PubMed Central
22. Motlagh, ME, Rabbani, A, Kelishadi, R, Mirmoghtadaee, P, Shahryari, S, Ardalan, G. Timing of puberty in Iranian girls according to their living area: a national study. J Res Med Sci 2011;16:276–81.Search in Google Scholar
23. Harley, KG, Berger, KP, Kogut, K, Parra, K, Lustig, RH, Greenspan, LC, et al.. Association of phthalates, parabens and phenols found in personal care products with pubertal timing in girls and boys. Hum Reprod 2019;34:109–17. https://doi.org/10.1093/humrep/dey337.Search in Google Scholar
24. Youn, I, Park, SH, Lim, IS, Kim, SJ. Ultrasound assessment of breast development: distinction between premature thelarche and precocious puberty. Am J Roentgenol 2015;204:620–4. https://doi.org/10.2214/ajr.14.12565.Search in Google Scholar
25. Bruserud, IS, Roelants, M, Oehme, NHB, Eide, GE, Bjerknes, R, Rosendahl, K, et al.. Ultrasound assessment of pubertal breast development in girls: intra-and interobserver agreement. Pediatr Radiol 2018;48:1576–83. https://doi.org/10.1007/s00247-018-4188-7.Search in Google Scholar
26. Venta, LA, Dudiak, CM, Salomon, CG, Flisak, ME. Sonographic evaluation of the breast. Radiographics 1994;14:29–50. https://doi.org/10.1148/radiographics.14.1.8128064.Search in Google Scholar
27. Valeur, NS, Rahbar, H, Chapman, T. Ultrasound of pediatric breast masses: what to do with lumps and bumps. Pediatr Radiol 2015;45:1584–99. https://doi.org/10.1007/s00247-015-3402-0.Search in Google Scholar
28. Neely, EK, Wilson, DM, Lee, PA, Stene, M, Hintz, RL. Spontaneous serum gonadotropin concentrations in the evaluation of precocious puberty. J Pediatr 1995;127:47–52. https://doi.org/10.1016/s0022-3476(95)70255-5.Search in Google Scholar
29. Houk, CP, Kunselman, AR, Lee, PA. Adequacy of a single unstimulated luteinizing hormone level to diagnose central precocious puberty in girls. Pediatrics 2009;123:1059–63. https://doi.org/10.1542/peds.2008-1180.Search in Google Scholar PubMed
30. Vurallı, D, Gönç, EN, Özön, ZA, Alikaşifoğlu, A. Adequacy of basal luteinizing hormone levels in the diagnosis of central precocious puberty. Turk Pediatri Ars 2020;55:131–8. https://doi.org/10.14744/TurkPediatriArs.2019.03708.Search in Google Scholar PubMed PubMed Central
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/jpem-2021-0181).
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