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

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

Breastfeeding and timing of pubertal onset in girls: a multiethnic population-based prospective cohort study

Authors: Sara Aghaee, Julianna Deardorff, Louise C. Greenspan, Charles P. Quesenberry Jr., Lawrence H. Kushi, Ai Kubo

Published in: BMC Pediatrics | Issue 1/2019

Login to get access

Abstract

Background

Early puberty is associated with higher risk of adverse health and behavioral outcomes throughout adolescence and adulthood. US girls are experiencing earlier puberty with substantial racial/ethnic differences. We examined the association between breastfeeding and pubertal timing to identify modifiable risk factors of early puberty and potential sources of racial/ethnic differences in the timing of pubertal development.

Methods

A prospective cohort study of 3331 racially/ethnically diverse girls born at Kaiser Permanente Northern California (KPNC) between 2004 and 06. All data were obtained from KPNC electronic clinical and administrative datasets. Mother-reported duration of breastfeeding was obtained from questionnaires administered at each ‘well-baby’ check-up exam throughout the baby’s first year and categorized as ‘Not breastfed’, ‘Breastfed < 6 months’, and ‘Breastfed ≥6 months’. Pubertal development data used Tanner stages assessed by pediatricians during routine pediatric checkups starting at age 6. Pubertal onset was defined as transition from Tanner Stage 1 to Tanner Stage 2+ for breast (thelarche) and pubic hair (pubarche). Weibull regression models accommodating for left, right, and interval censoring were used in all analyses. Models were adjusted for maternal age, education, race/ethnicity, parity and prepubertal body mass index (BMI). We also examined race/ethnicity as a potential effect modifier of these associations.

Results

Not breastfeeding was associated with earlier onset of breast and pubic hair development compared to breastfeeding ≥6 months (adjusted hazard ratio [HR]: 1.25; 95% confidence interval [CI]: 1.07–1.46; HR: 1.24; 95% CI: 1.05–1.46, respectively). Breastfeeding for < 6 months was also associated with the risk of earlier pubic hair development (HR: 1.14; 95% CI: 1.00–1.30, compared to breastfeeding ≥6 months). Inclusion of girls’ prepubertal BMI slightly attenuated the association between breastfeeding and timing of breast onset but remained significant. The association between not breastfeeding and early breast development may be stronger among African American girls (HR: 1.92; 95% CI: 1.01–3.66, compared to breastfeeding ≥6 months) than other racial/ethnic groups.

Conclusions

Breastfeeding is an independent predictor of pubertal onset in girls, and the strength of the association may vary by race/ethnicity. Providing breastfeeding support and lactation education for high risk mothers may help prevent earlier pubertal onset and promote positive health outcomes later in life.
Literature
1.
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;132:1019–27.CrossRefPubMedPubMedCentral 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;132:1019–27.CrossRefPubMedPubMedCentral
2.
go back to reference Golub MS, Collman GW, Foster PM, Kimmel CA, Rajpert-De Meyts E, Reiter EO, Sharpe RM, Skakkebaek NE, Toppari J. Public health implications of altered puberty timing. Pediatrics. 2008;121(Suppl 3):S218–30.CrossRefPubMed Golub MS, Collman GW, Foster PM, Kimmel CA, Rajpert-De Meyts E, Reiter EO, Sharpe RM, Skakkebaek NE, Toppari J. Public health implications of altered puberty timing. Pediatrics. 2008;121(Suppl 3):S218–30.CrossRefPubMed
3.
go back to reference Downing J, Bellis MA. Early pubertal onset and its relationship with sexual risk taking, substance use and anti-social behaviour: a preliminary cross-sectional study. BMC Public Health. 2009;9:446.CrossRefPubMedPubMedCentral Downing J, Bellis MA. Early pubertal onset and its relationship with sexual risk taking, substance use and anti-social behaviour: a preliminary cross-sectional study. BMC Public Health. 2009;9:446.CrossRefPubMedPubMedCentral
4.
go back to reference Wang H, Lin SL, Leung GM, Schooling CM. Age at onset of puberty and adolescent depression: “children of 1997” birth cohort. Pediatrics. 2016;137(6):e20153231.CrossRefPubMed Wang H, Lin SL, Leung GM, Schooling CM. Age at onset of puberty and adolescent depression: “children of 1997” birth cohort. Pediatrics. 2016;137(6):e20153231.CrossRefPubMed
5.
go back to reference Cance JD, Ennett ST, Morgan-Lopez AA, Foshee VA, Talley AE. Perceived pubertal timing and recent substance use among adolescents: a longitudinal perspective. Addiction. 2013;108:1845–54.CrossRefPubMedPubMedCentral Cance JD, Ennett ST, Morgan-Lopez AA, Foshee VA, Talley AE. Perceived pubertal timing and recent substance use among adolescents: a longitudinal perspective. Addiction. 2013;108:1845–54.CrossRefPubMedPubMedCentral
6.
go back to reference Dudovitz RN, Chung PJ, Elliott MN, Davies SL, Tortolero S, Baumler E, Banspach SW, Schuster MA. Relationship of age for grade and pubertal stage to early initiation of substance use. Prev Chronic Dis. 2015;12:E203.CrossRefPubMedPubMedCentral Dudovitz RN, Chung PJ, Elliott MN, Davies SL, Tortolero S, Baumler E, Banspach SW, Schuster MA. Relationship of age for grade and pubertal stage to early initiation of substance use. Prev Chronic Dis. 2015;12:E203.CrossRefPubMedPubMedCentral
7.
go back to reference Udry JR. Age at menarche, at first intercourse, and at first pregnancy. J Biosoc Sci. 1979;11:433–41.CrossRefPubMed Udry JR. Age at menarche, at first intercourse, and at first pregnancy. J Biosoc Sci. 1979;11:433–41.CrossRefPubMed
8.
go back to reference Dossus L, Allen N, Kaaks R, Bakken K, Lund E, Tjonneland A, Olsen A, Overvad K, Clavel-Chapelon F, Fournier A, et al. Reproductive risk factors and endometrial cancer: the European prospective investigation into cancer and nutrition. Int J Cancer. 2010;127:442–51. Dossus L, Allen N, Kaaks R, Bakken K, Lund E, Tjonneland A, Olsen A, Overvad K, Clavel-Chapelon F, Fournier A, et al. Reproductive risk factors and endometrial cancer: the European prospective investigation into cancer and nutrition. Int J Cancer. 2010;127:442–51.
9.
go back to reference McDowell MA, Brody DJ, Hughes JP. Has age at menarche changed? Results from the National Health and Nutrition Examination Survey (NHANES) 1999-2004. J Adolesc Health. 2007;40:227–31.CrossRefPubMed McDowell MA, Brody DJ, Hughes JP. Has age at menarche changed? Results from the National Health and Nutrition Examination Survey (NHANES) 1999-2004. J Adolesc Health. 2007;40:227–31.CrossRefPubMed
10.
go back to reference Singh GK, Kogan MD, Dee DL. Nativity/immigrant status, race/ethnicity, and socioeconomic determinants of breastfeeding initiation and duration in the United States, 2003. Pediatrics. 2007;119:S38–46.CrossRefPubMed Singh GK, Kogan MD, Dee DL. Nativity/immigrant status, race/ethnicity, and socioeconomic determinants of breastfeeding initiation and duration in the United States, 2003. Pediatrics. 2007;119:S38–46.CrossRefPubMed
11.
go back to reference Centers for Disease Control and Prevention. Progress in increasing breastfeeding and reducing racial/ethnic differences-United States, 2000–2008 births. MMWR Morb Mortal Wkly Rep. 2013;62:77. Centers for Disease Control and Prevention. Progress in increasing breastfeeding and reducing racial/ethnic differences-United States, 2000–2008 births. MMWR Morb Mortal Wkly Rep. 2013;62:77.
12.
13.
go back to reference Kale A, Deardorff J, Lahiff M, Laurent C, Greenspan LC, Hiatt RA, Windham G, Galvez MP, Biro FM, Pinney SM. Breastfeeding versus formula-feeding and girls’ pubertal development. Matern Child Health J. 2015;19:519–27.CrossRefPubMedPubMedCentral Kale A, Deardorff J, Lahiff M, Laurent C, Greenspan LC, Hiatt RA, Windham G, Galvez MP, Biro FM, Pinney SM. Breastfeeding versus formula-feeding and girls’ pubertal development. Matern Child Health J. 2015;19:519–27.CrossRefPubMedPubMedCentral
14.
go back to reference Lee HA, Kim YJ, Lee H, Gwak HS, Hong YS, Kim HS, Park EA, Cho SJ, Ha EH, Park H. The preventive effect of breast-feeding for longer than 6 months on early pubertal development among children aged 7–9 years in Korea. Public Health Nutr. 2015;18:3300–7.CrossRefPubMed Lee HA, Kim YJ, Lee H, Gwak HS, Hong YS, Kim HS, Park EA, Cho SJ, Ha EH, Park H. The preventive effect of breast-feeding for longer than 6 months on early pubertal development among children aged 7–9 years in Korea. Public Health Nutr. 2015;18:3300–7.CrossRefPubMed
16.
go back to reference Blell M, Pollard TM, Pearce MS. Predictors of age at menarche in the Newcastle thousand families study. J Biosoc Sci. 2008;40:563–75.CrossRefPubMed Blell M, Pollard TM, Pearce MS. Predictors of age at menarche in the Newcastle thousand families study. J Biosoc Sci. 2008;40:563–75.CrossRefPubMed
17.
18.
go back to reference Karaolis-Danckert N, Buyken AE, Sonntag A, Kroke A. Birth and early life influences on the timing of puberty onset: results from the DONALD (DOrtmund nutritional and anthropometric longitudinally designed) study. Am J Clin Nutr. 2009;90:1559–65.CrossRefPubMed Karaolis-Danckert N, Buyken AE, Sonntag A, Kroke A. Birth and early life influences on the timing of puberty onset: results from the DONALD (DOrtmund nutritional and anthropometric longitudinally designed) study. Am J Clin Nutr. 2009;90:1559–65.CrossRefPubMed
19.
go back to reference Novotny R, Daida Y, Grove J, Acharya S, Vogt T. Formula feeding in infancy is associated with adolescent body fat and earlier menarche. Cell Mol Biol (Noisy-le-grand). 2003;49:1289–93. Novotny R, Daida Y, Grove J, Acharya S, Vogt T. Formula feeding in infancy is associated with adolescent body fat and earlier menarche. Cell Mol Biol (Noisy-le-grand). 2003;49:1289–93.
20.
go back to reference Merzenich H, Boeing H, Wahrendorf J. Dietary fat and sports activity as determinants for age at menarche. Am J Epidemiol. 1993;138:217–24.CrossRefPubMed Merzenich H, Boeing H, Wahrendorf J. Dietary fat and sports activity as determinants for age at menarche. Am J Epidemiol. 1993;138:217–24.CrossRefPubMed
21.
go back to reference Moisan J, Meyer F, Gingras S. A nested case-control study of the correlates of early menarche. Am J Epidemiol. 1990;132:953–61.CrossRefPubMed Moisan J, Meyer F, Gingras S. A nested case-control study of the correlates of early menarche. Am J Epidemiol. 1990;132:953–61.CrossRefPubMed
22.
go back to reference Kingston D, Heaman M, Fell D, Chalmers B, System MESGotCPS. Comparison of adolescent, young adult, and adult women’s maternity experiences and practices. Pediatrics. 2012;129:e1228–37.CrossRefPubMed Kingston D, Heaman M, Fell D, Chalmers B, System MESGotCPS. Comparison of adolescent, young adult, and adult women’s maternity experiences and practices. Pediatrics. 2012;129:e1228–37.CrossRefPubMed
23.
go back to reference Chen X-K, Wen SW, Fleming N, Demissie K, Rhoads GG, Walker M. Teenage pregnancy and adverse birth outcomes: a large population based retrospective cohort study. Int J Epidemiol. 2007;36:368–73.CrossRefPubMed Chen X-K, Wen SW, Fleming N, Demissie K, Rhoads GG, Walker M. Teenage pregnancy and adverse birth outcomes: a large population based retrospective cohort study. Int J Epidemiol. 2007;36:368–73.CrossRefPubMed
24.
go back to reference Blondel B, Kogan MD, Alexander GR, Dattani N, Kramer MS, Macfarlane A, Wen SW. The impact of the increasing number of multiple births on the rates of preterm birth and low birthweight: an international study. Am J Public Health. 2002;92:1323–30.CrossRefPubMedPubMedCentral Blondel B, Kogan MD, Alexander GR, Dattani N, Kramer MS, Macfarlane A, Wen SW. The impact of the increasing number of multiple births on the rates of preterm birth and low birthweight: an international study. Am J Public Health. 2002;92:1323–30.CrossRefPubMedPubMedCentral
25.
go back to reference World Health Organization. Global strategy for infant and young child feeding. The optimal duration of exclusive breastfeeding. Geneva: WHO; 2001. World Health Organization. Global strategy for infant and young child feeding. The optimal duration of exclusive breastfeeding. Geneva: WHO; 2001.
26.
go back to reference Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Childh. 1969;44:291–303.CrossRefPubMed Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Childh. 1969;44:291–303.CrossRefPubMed
27.
go back to reference Kubo A, Deardorff J, Laurent CA, Ferrara A, Greenspan LC, Quesenberry CP, Kushi LH. Associations between maternal obesity and pregnancy hyperglycemia and timing of pubertal onset in adolescent girls: a population-based study. Am J Epidemiol. 2018;187(7):1362–69.CrossRefPubMedPubMedCentral Kubo A, Deardorff J, Laurent CA, Ferrara A, Greenspan LC, Quesenberry CP, Kushi LH. Associations between maternal obesity and pregnancy hyperglycemia and timing of pubertal onset in adolescent girls: a population-based study. Am J Epidemiol. 2018;187(7):1362–69.CrossRefPubMedPubMedCentral
28.
go back to reference Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL. CDC growth charts for the United States: methods and development. In: Vital and health statistics Series 11, Data from the national health survey, vol. 2002; 2000. p. 1–190. Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL. CDC growth charts for the United States: methods and development. In: Vital and health statistics Series 11, Data from the national health survey, vol. 2002; 2000. p. 1–190.
29.
go back to reference Deardorff J, Abrams B, Ekwaru JP, Rehkopf DH. Socioeconomic status and age at menarche: an examination of multiple indicators in an ethnically diverse cohort. Ann Epidemiol. 2014;24:727–33.CrossRefPubMedPubMedCentral Deardorff J, Abrams B, Ekwaru JP, Rehkopf DH. Socioeconomic status and age at menarche: an examination of multiple indicators in an ethnically diverse cohort. Ann Epidemiol. 2014;24:727–33.CrossRefPubMedPubMedCentral
30.
go back to reference Heck KE, Braveman P, Cubbin C, Chávez GF, Kiely JL. Socioeconomic status and breastfeeding initiation among California mothers. Public Health Rep. 2006;121:51–9.CrossRefPubMedPubMedCentral Heck KE, Braveman P, Cubbin C, Chávez GF, Kiely JL. Socioeconomic status and breastfeeding initiation among California mothers. Public Health Rep. 2006;121:51–9.CrossRefPubMedPubMedCentral
31.
go back to reference Thulier D, Mercer J. Variables associated with breastfeeding duration. J Obstet Gynecol Neonatal Nurs. 2009;38:259–68.CrossRefPubMed Thulier D, Mercer J. Variables associated with breastfeeding duration. J Obstet Gynecol Neonatal Nurs. 2009;38:259–68.CrossRefPubMed
32.
go back to reference Windham GC, Zhang L, Longnecker MP, Klebanoff M. Maternal smoking, demographic and lifestyle factors in relation to daughter’s age at menarche. Paediatr Perinat Epidemiol. 2008;22:551–61.CrossRefPubMedPubMedCentral Windham GC, Zhang L, Longnecker MP, Klebanoff M. Maternal smoking, demographic and lifestyle factors in relation to daughter’s age at menarche. Paediatr Perinat Epidemiol. 2008;22:551–61.CrossRefPubMedPubMedCentral
33.
go back to reference Lucas A, Boyes S, Bloom S, Aynsley-Green A. Metabolic and endocrine responses to a milk feed in six-day-old term infants: differences between breast and cow's milk formula feeding. Acta Paediatr. 1981;70:195–200.CrossRef Lucas A, Boyes S, Bloom S, Aynsley-Green A. Metabolic and endocrine responses to a milk feed in six-day-old term infants: differences between breast and cow's milk formula feeding. Acta Paediatr. 1981;70:195–200.CrossRef
34.
go back to reference Lawrence RA. Does breastfeeding protect against overweight and obesity in children? A review. Child Obes. 2010;6:193–7.CrossRef Lawrence RA. Does breastfeeding protect against overweight and obesity in children? A review. Child Obes. 2010;6:193–7.CrossRef
35.
go back to reference Dewey KG. Cross-cultural patterns of growth and nutritional status of breast-fed infants. Am J Clin Nutr. 1998;67:10–7.CrossRefPubMed Dewey KG. Cross-cultural patterns of growth and nutritional status of breast-fed infants. Am J Clin Nutr. 1998;67:10–7.CrossRefPubMed
36.
go back to reference Belsky J, Houts RM, Pasco Fearon R. Infant attachment security and the timing of puberty: testing an evolutionary hypothesis. Psychol Sci. 2010;21:1195–201.CrossRefPubMed Belsky J, Houts RM, Pasco Fearon R. Infant attachment security and the timing of puberty: testing an evolutionary hypothesis. Psychol Sci. 2010;21:1195–201.CrossRefPubMed
37.
go back to reference Tharner A, Luijk MP, Raat H, IJzendoorn MH, Bakermans-Kranenburg MJ, Moll HA, Jaddoe VW, Hofman A, Verhulst FC, Tiemeier H. Breastfeeding and its relation to maternal sensitivity and infant attachment. J Dev Behav Pediatr. 2012;33:396–404.CrossRefPubMed Tharner A, Luijk MP, Raat H, IJzendoorn MH, Bakermans-Kranenburg MJ, Moll HA, Jaddoe VW, Hofman A, Verhulst FC, Tiemeier H. Breastfeeding and its relation to maternal sensitivity and infant attachment. J Dev Behav Pediatr. 2012;33:396–404.CrossRefPubMed
38.
go back to reference Grigoriadis S, VonderPorten EH, Mamisashvili L, Tomlinson G, Dennis C-L, Koren G, Steiner M, Mousmanis P, Cheung A, Radford K. The impact of maternal depression during pregnancy on perinatal outcomes: a systematic review and meta-analysis; 2013.CrossRef Grigoriadis S, VonderPorten EH, Mamisashvili L, Tomlinson G, Dennis C-L, Koren G, Steiner M, Mousmanis P, Cheung A, Radford K. The impact of maternal depression during pregnancy on perinatal outcomes: a systematic review and meta-analysis; 2013.CrossRef
39.
go back to reference Kiernan K, Pickett KE. Marital status disparities in maternal smoking during pregnancy, breastfeeding and maternal depression. Soc Sci Med. 2006;63:335–46.CrossRefPubMed Kiernan K, Pickett KE. Marital status disparities in maternal smoking during pregnancy, breastfeeding and maternal depression. Soc Sci Med. 2006;63:335–46.CrossRefPubMed
40.
go back to reference Ellis BJ, Garber J. Psychosocial antecedents of variation in girls’ pubertal timing: maternal depression, stepfather presence, and marital and family stress. Child Dev. 2000;71:485–501.CrossRefPubMed Ellis BJ, Garber J. Psychosocial antecedents of variation in girls’ pubertal timing: maternal depression, stepfather presence, and marital and family stress. Child Dev. 2000;71:485–501.CrossRefPubMed
Metadata
Title
Breastfeeding and timing of pubertal onset in girls: a multiethnic population-based prospective cohort study
Authors
Sara Aghaee
Julianna Deardorff
Louise C. Greenspan
Charles P. Quesenberry Jr.
Lawrence H. Kushi
Ai Kubo
Publication date
01-12-2019
Publisher
BioMed Central
Keywords
Obesity
Obesity
Published in
BMC Pediatrics / Issue 1/2019
Electronic ISSN: 1471-2431
DOI
https://doi.org/10.1186/s12887-019-1661-x

Other articles of this Issue 1/2019

BMC Pediatrics 1/2019 Go to the issue