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Onset of Breast Development in a Longitudinal Cohort
Open accessAbstract
BACKGROUND AND OBJECTIVES: There is growing evidence of pubertal maturation occurring at earlier ages, with many studies based on cross-sectional observations. This study examined age at onset of breast development (thelarche), and the impact of BMI and race/ethnicity, in the 3 puberty study sites of the Breast Cancer and the Environment Research Program, a prospective cohort of >1200 girls. METHODS: Girls, 6 to 8 years at enrollment, were followed longitudinally at regular intervals from 2004 to 2011 in 3 geographic areas: the San Francisco Bay Area, Greater Cincinnati, and New York City. Sexual maturity assessment using Tanner staging was conducted by using standardized observation and palpation methods by trained and certified staff. Kaplan-Meier analyses were used to describe age at onset of breast maturation by covariates. RESULTS: The age at onset of breast stage 2 varied by race/ethnicity, BMI at baseline, and site. Median age at onset of breast stage 2 was 8.8, 9.3, 9.7, and 9.7 years for African American, Hispanic, white non-Hispanic, and Asian participants, respectively. Girls with greater BMI reached breast stage 2 at younger ages. Age-specific and standardized prevalence of breast maturation was contrasted to observations in 2 large cross-sectional studies conducted 10 to 20 years earlier (Pediatric Research in Office Settings and National Health and Nutrition Examination Survey III) and found to have occurred earlier among white, non-Hispanic, but not African American girls. CONCLUSIONS: We observed the onset of thelarche at younger ages than previously documented, with important differences associated with race/ethnicity and BMI, confirming and extending patterns seen previously. These findings are consistent with temporal changes in BMI.
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In the citing paper
“Pubertal onset is also occurring earlier in developed nations, particularly in unserved populations”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Biro et al., 2013
In the citing paper
“Over the last decades, the average age at puberty onset in girls has advanced by multiple years”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Biro et al., 2013
In the citing paper
“In one study, the mean age of breast budding in black or Hispanic girls occurred at 8.8 and 9.3 years old (respectively) compared to 9.7 in white or Asian girls”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Biro et al., 2013
In the citing paper
“In North American boys and girls, earlier maturation is more common in black, Hispanic and low socioeconomic status children”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Biro et al., 2013
In the citing paper
“Black girls enter puberty at younger ages than their White, Latinx, and Asian American counterparts and spend longer periods in the pubertal transition than Black girls in previous generations (Biro et al., 2013;Dorn, Dahl, Woodward, & Biro, 2006;Herman-Giddens et al., 1997).”
From Ethnic‐Racial Socialization Among Mothers of Black and Black‐White Biracial Daughters During the Pubertal Transition (2022) · cites this paper as Biro et al., 2013
In the citing paper
“Black girls enter puberty at younger ages than their White, Latinx, and Asian American counterparts and spend longer periods in the pubertal transition than Black girls in previous generations (Biro et al., 2013;Dorn, Dahl, Woodward, & Biro, 2006;Herman-Giddens et al., 1997).”
From Ethnic‐Racial Socialization Among Mothers of Black and Black‐White Biracial Daughters During the Pubertal Transition (2022) · cites this paper as Biro et al., 2013
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Citations
Cites
Variations in pattern of pubertal changes in girls
Marshall, W. A., & Tanner, J. M. (1969) · Archives of Disease in Childhood · doi:10.1136/adc.44.235.291 · Cited by 5,963
Renehan, A. G., Tyson, M., Egger, M., Heller, R. F., & Zwahlen, M. (2008) · The Lancet · doi:10.1016/s0140-6736(08)60269-x · Cited by 5,219
Prevalence of obesity and trends in body mass index among US children and adolescents, 1999-2010.
Ogden, C., Carroll, M., Kit, B., & Flegal, K. (2012) · Journal of the American Medical Association (JAMA) · doi:10.1001/jama.2012.40 · Cited by 4,128
High body mass index for age among US children and adolescents, 2003-2006.
Ogden, C. L. (2008) · JAMA · doi:10.1001/jama.299.20.2401 · Cited by 1,850
Parent, A.-S., Teilmann, G., Juul, A., Skakkebaek, N. E., Toppari, J., & Bourguignon, J.-P. (2003) · Endocrine Reviews · doi:10.1210/er.2002-0019 · Cited by 1,762
Herman-Giddens, M. E., Slora, E. J., Wasserman, R. C., Bourdony, C. J., Bhapkar, M. V., Koch, G. G., & Hasemeier, C. M. (1997) · PEDIATRICS · doi:10.1542/peds.99.4.505 · Cited by 1,709
Earlier Onset of Puberty in Girls: Relation to Increased Body Mass Index and Race
Kaplowitz, P. B., Slora, E. J., Wasserman, R. C., Pedlow, S. E., & Herman‐Giddens, M. E. (2001) · PEDIATRICS · doi:10.1542/peds.108.2.347 · Cited by 745
Link Between Body Fat and the Timing of Puberty
Kaplowitz, P. B. (2008) · Pediatrics · doi:10.1542/peds.2007-1813f · Cited by 710
Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings
Euling, S. Y., Herman-Giddens, M. E., Lee, P. A., Selevan, S. G., Juul, A., SØrensen, T. I. A., Dunkel, L., Himes, J. H., Teilmann, G., & Swan, S. H. (2008) · PEDIATRICS · doi:10.1542/peds.2007-1813d · Cited by 662
Recent decline in age at breast development: The Copenhagen Puberty Study
Aksglaede, L., Sørensen, K., Petersen, J. H., Skakkebæk, N. E., & Juul, A. (2009) · Pediatrics · doi:10.1542/peds.2008-2491 · Cited by 626
Thelarche, pubarche, and menarche attainment in children with normal and elevated body mass index
Rosenfield, R. L., Lipton, R. B., & Drum, M. L. (2009) · PEDIATRICS · doi:10.1542/peds.2008-0146 · Cited by 499
Obesity and the pubertal transition in girls and boys
Solorzano, C. M. B., & McCartney, C. R. (2010) · Reproduction · doi:10.1530/rep-10-0119 · Cited by 454
Is Pubertal Timing Associated With Psychopathology in Young Adulthood?
Graber, J. A., Seeley, J. R., Jeanne Brooks-gunn, B., & Lewinsohn, P. M. (2004) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/01.chi.0000120022.14101.11 · Cited by 418
Childhood obesity and the timing of puberty
Ahmed, M. L., Ong, K. K., & Dunger, D. B. (2009) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2009.02.004 · Cited by 409
Evolution, development and timing of puberty
Gluckman, P. D., & Hanson, M. A. (2005) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2005.11.006 · Cited by 408
Coming of Age Too Early: Pubertal Influences on Girls' Vulnerability to Psychological Distress
Ge, X., Conger, R. D., & Elder, G. H. (1996) · Child Development · doi:10.1111/j.1467-8624.1996.tb01919.x · Cited by 387
Coming of age too early: pubertal influences on girls' vulnerability to psychological distress
Ge, X., Conger, R. D., & Elder, G. H. (1996) · Child Development · doi:10.2307/1131784 · Cited by 381
Pubertal assessment method and baseline characteristics in a mixed longitudinal study of girls
Biro, F. M., Galvez, M. P., Greenspan, L. C., Succop, P. A., Vangeepuram, N., Pinney, S. M., Teitelbaum, S., Windham, G. C., Kushi, L. H., & Wolff, M. S. (2010) · Pediatrics · doi:10.1542/peds.2009-3079 · Cited by 348
Self-citationWeight Status in Young Girls and the Onset of Puberty
Lee, J. M., Appugliese, D. P., Kaciroti, N., CORWYN, R. F., Bradley, R. H., & Lumeng, J. C. (2007) · PEDIATRICS · doi:10.1542/peds.2006-2188 · Cited by 347
Environmental Factors and Puberty Timing: Expert Panel Research Needs
Louis, G. M. B., Gray, L. E., Marcus, M., Ojeda, S. R., Pescovitz, O. H., Witchel, S. F., Sippell, W. G., Abbott, D. H., Soto, A. M., Tyl, R. W., et al. (2008) · PEDIATRICS · doi:10.1542/peds.1813e · Cited by 334
Percent Body Fat at Age 5 Predicts Earlier Pubertal Development Among Girls at Age 9
Davison, K. K., Susman, E. J., & Birch, L. L. (2003) · PEDIATRICS · doi:10.1542/peds.111.4.815 · Cited by 319
On the use and utility of the Weibull model in the analysis of survival data
Carroll, K. J. (2003) · Controlled Clinical Trials · doi:10.1016/s0197-2456(03)00072-2 · Cited by 295
Outcomes of early pubertal timing in young women: a prospective population-based study
Copeland, W., Shanahan, L., Miller, S., Costello, E. J., Angold, A., & Maughan, B. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2010.09081190 · Cited by 271
Adolescent Obesity and Puberty: The “Perfect Storm”
Jasik, C. B., & Lustig, R. H. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1429.009 · Cited by 270
Frontini, M., Srinivasan, S. R., & Berenson, G. S. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.0802422 · Cited by 218
Reproductive Factors and Risk of Endometrial Cancer The Iowa Women's Health Study
McPherson, C. P., Sellers, T. A., Potter, J. D., Bostick, R. M., & FOLSOM, A. R. (1996) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a008707 · Cited by 217
Early puberty and adolescent pregnancy: The influence of alcohol use
Deardorff, J., Gonzales, N. A., Christopher, F. S., Roosa, M. W., & Millsap, R. E. (2005) · Pediatrics · doi:10.1542/peds.2005-0542 · Cited by 185
Growing up Fast: Stress Exposure and Subjective “Weathering” in Emerging Adulthood
Foster, H., Hagan, J. L., & Jeanne Brooks-gunn, B. (2008) · Journal of Health and Social Behavior · doi:10.1177/002214650804900204 · Cited by 183
Harnack, L., Fulkerson, J. A., & Robien, K. (2008) · Cited by 183
Reproductive factors and risk of endometrial cancer
Parazzini, F., Vecchia, C. L., Negri, E., Fedele, L., & Balotta, F. (1991) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(11)80012-8 · Cited by 176
Buyken, A. E., Karaolis‐Danckert, N., & Remer, T. (2008) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.26733 · Cited by 138
Timing of maturation and predictors of menarche in girls enrolled in a contemporary British cohort
Rubin, C., Maisonet, M., Kieszak, S. M., Monteilh, C. P., Holmes, A. K., Flanders, D. W., Heron, J., Golding, J., McGeehin, M., & Marcus, M. (2009) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2009.01055.x · Cited by 132
Age at menarche, urine estrogens and breast cancer risk
MacMahon, B., Trichopoulos, D., Brown, J., Andersen, A. P., Cole, P. T., Dewaard, F., Kauraniemi, T. V., Polychronopoulou, A., Ravnihar, B., Stormby, N., et al. (1982) · International Journal of Cancer · doi:10.1002/ijc.2910300408 · Cited by 128
Ovarian Cancer Risk Factors in African-American and White Women
Moorman, P. G., Weber, R. P., Akushevich, L., Berchuck, A., & Schildkraut, J. M. (2009) · American Journal of Epidemiology · doi:10.1093/aje/kwp176 · Cited by 116
Clavel‐Chapelon, F. (2002) · Cancer Causes & Control · doi:10.1023/a:1020684821837 · Cited by 99
Striegel‐Moore, R. H., McMahon, R. P., Biro, F. M., Schreiber, G. B., Crawford, P. B., & Voorhees, C. C. (2001) · International Journal of Eating Disorders · doi:10.1002/eat.1103 · Cited by 99
Putting pubertal timing in developmental context: Implications for prevention
Graber, J. A., Nichols, T. R., & Jeanne Brooks-gunn, B. (2010) · Developmental Psychobiology · doi:10.1002/dev.20438 · Cited by 96
Very Long-Term Follow-Up of Girls with Early and Late Menarche
Johansson, T., & Ritzén, E. M. (2005) · KARGER eBooks · doi:10.1159/000084098 · Cited by 91
Hiatt, R. A., Haslam, S. Z., & Osuch, J. R. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.0800120 · Cited by 90
Li, C. I., Littman, A. J., & White, E. (2007) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-07-0242 · Cited by 61
Maternal smoking, demographic and lifestyle factors in relation to daughter's age at menarche
Windham, G. C., Zhang, L., Longnecker, M. P., & Klebanoff, M. A. (2008) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2008.00948.x · Cited by 60
Heger, S., Körner, A., Meigen, C., Gausche, R., Keller, A., Keller, E., & Kiess, W. (2008) · Journal of Pediatric Endocrinology and Metabolism · doi:10.1515/jpem.2008.21.9.865 · Cited by 38
Growth patterns and the risk of breast cancer in women
Ahlgren, M., Melbye, M., Wohlfahrt, J., & Sørensen, T. I. A. (2006) · International Journal of Gynecological Cancer · doi:10.1111/j.1525-1438.2006.00698.x · Cited by 36
Aspiration cytology in the staging of urologic cancer
Piscioli, F., Scappini, P., & Luciani, L. (1985) · Cancer · doi:10.1002/1097-0142(19850901)56:5 · Cited by 28
Puberty as a Window of Susceptibility
Biro, F. M., & Wolff, M. S. (2011) · Springer eBooks · doi:10.1007/978-1-4419-9896-5_2 · Cited by 16
Russo, J. (2011) · Springer eBooks · doi:10.1007/978-1-4419-9896-5 · Cited by 10
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Yuan, M., Cross, S. J., Loughlin, S. E., & Leslie, F. M. (2015) · The Journal of Physiology · doi:10.1113/jp270492 · Cited by 623
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Clinical Management of Congenital Hypogonadotropic Hypogonadism
Young, J., Xu, C., Papadakis, G. E., Acierno, J. S., Maione, L., Hietamäki, J., Raivio, T., & Pitteloud, N. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00116 · Cited by 421
Metadata
- Authors
- Biro, F. M., Greenspan, L. C., Galvez, M. P., Pinney, S. M., Teitelbaum, S., Windham, G. C., Deardorff, J., Herrick, R. L., Succop, P. A., Hiatt, R. A., Kushi, L. H., & Wolff, M. S.
- Affiliations
- Cincinnati Children's Hospital Medical Center (US)
- Kaiser Permanente (US)
- Department of Preventive Medicine, and
- University of Cincinnati (US)
- California Department of Public Health (US)
- University of California, Berkeley (US)
- University of California, San Francisco (US)
- Icahn School of Medicine at Mount Sinai (US)
- ORCID
- Venue
- PEDIATRICS
- Publisher
- American Academy of Pediatrics (AAP)
- Published
- 2013-12-01
- Volume
- 132
- Issue
- 6
- Pages
- 1019-1027
- ISSN
- 0031-4005 (ISSN-L)
- 1098-4275
- PMC
- PMC3838525
- OpenAlex
- W2113207708
- Cited by
- 362
- References
- 45
- Citations by year
- 2026: 13 · 2025: 20 · 2024: 26 · 2023: 21 · 2022: 48 · 2021: 33 · 2020: 42 · 2019: 30 · 2018: 26 · 2017: 31 · 2016: 32 · 2015: 19 · 2014: 18 · 2013: 2
- FWCI
- 28.58
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- PEDIATRICS (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Kaiser Permanente
- Michigan State University
- University of Cincinnati
- National Institutes of Health (5ul1rr026314-03, UL1TR000077)
- National Institute of Environmental Health Sciences (P01ES009584, U01ES012800, U01ES019457, U01ES012771, T32-ES 10957, U01ES012770, P30ES006096, U01ES019435, U01ES019453, U01ES012801, U01ES019454, T32ES010957)
- National Center for Research Resources (UL1RR024131, UL1RR029887, UL1-RR026314, CSTA-UL1RR026314, CSTA-UL1RR029887)
- National Center for Chronic Disease Prevention and Health Promotion
- National Center for Advancing Translational Sciences
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Oncology › Cancer Risks and Factors
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Adolescent Sexual and Reproductive Health
- Keywords
- thelarche, breast development, puberty onset, pubertal timing, body mass index, racial and ethnic differences, African American girls, Hispanic girls, Tanner stages, longitudinal cohort, childhood obesity
- MeSH terms
- Adolescent, Age Factors, Breast, Child, Female, Humans, Longitudinal Studies, New York City, Ohio, Prospective Studies, Puberty, San Francisco, Body Mass Index, Linear Models, Kaplan-Meier Estimate
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