Mini-Review
Puberty in Girls of the 21st Century

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Abstract

Several studies have noted contemporary girls are undergoing pubertal maturation at younger ages. During this same time period many Western nations have experienced an obesity epidemic, prompting investigators and public health officials to consider the association of these 2 events, and if other exposures might impact this relationship. There are several potential mechanisms that could impact the relationship of pubertal timing in girls with greater body mass, including direct effects of obesity on pubertal timing as well underlying exposures that impact body mass as well as timing of pubertal maturation. These underlying conditions include chemical compounds that could impact synthesis or action of sex hormones, called endocrine disrupting chemicals (EDs). We examine the decline in the age of breast development and potential genetic and environmental influences, the obesity epidemic in the US and other nations, and potential mechanisms to explain the relationship between greater body mass index with earlier puberty in girls.

Introduction

A group of experts in puberty and public health were convened by the Environmental Protection Agency and the National Institute of Environmental Health Sciences, and examined the data over the past several decades regarding timing of puberty. They concluded that girls are experiencing earlier breast development.1 There appear to be several factors to account for these changes, which include an association between elevated body mass index and earlier timing of puberty (vide infra), prompting some to consider the recent changes in adolescent obesity and pubertal timing as the “perfect storm.”2 It appears that girls of the 21st century are indeed experiencing a perfect storm, with an evolutionary drive for energy conservation; a mismatch in energy balance through greater consumption of calorically dense foods and decreased energy expenditure, reflecting recent trends in physical activities; and a contemporary chemical cocktail with greater levels of exposure to endocrine-disrupting chemicals and obesogens. This paper will examine the decline in the age of breast development and potential genetic and environmental influences, the obesity epidemic in the US and other nations, and potential mechanisms to explain the relationship between greater body mass index with earlier puberty in girls.

The timing of puberty may serve as a sensitive indicator of environmental factors.3 Age of onset of puberty and age of menarche dropped in the first half of the 20th century; as noted in Table 1,4, 5, 6, 7, 8, 9, 10, 11, 12 age of onset of breast development appears to have declined over the second half of the twentieth century as well. A panel of experts concluded that there were sufficient data to note a trend in earlier onset of breast development in the US over the second half of the 20th century.1 Similarly, the Copenhagen Puberty Study reported that girls matured 1 year earlier than a comparable cohort born 15-16 years earlier,5 and Caucasian girls at ages 7 and 8 in the Breast Cancer and the Environment Program13 were more mature than girls born 15 years earlier from the Pediatric Research in Office Settings (PROS) Study.8 Age of menarche has not dropped as much; in examining nationally representative data generated through NHANES, women born in the 1980s reported age of menarche 0.2-0.4 years earlier than those born in the 1950s.1, 14 Although the correlation between age at onset of breast development and age of menarche was high several decades ago (correlation up to 0.90), it appears that this correlation has decreased among more recent cohorts (correlation around 0.40), suggesting there is less shared variance between onset of breast development and age of menarche.15 Given a limited opportunity for genetic changes, the change in correlation most likely represents environmental or gene/environment interactions (including epigenetic changes).

As noted earlier, natural selection appears to favor earlier reproductive development and both a thrifty genotype16 and a thrifty phenotype.17 Our genes evolved during times when procurement of food was more difficult, leading to genetic changes that promoted thrifty genotypes and phenotypes in response to harsh times.18, 19 This “developmental plasticity,” impacted by environmental exposures during sensitive developmental periods, is associated with greater obesity as well as other metabolic and physiologic consequences.20 Bouchard, examining those genes associated with obesity, as well as observing behavioral and biologic traits which optimized energy storage, proposed 5 major classes of genotypes that favored energy conservation. These are the thrifty genotype (low basal metabolic rate, low thermogenesis); hyperphagic genotype (poor regulation of appetite and satiety); sedens genotype (propensity to physical inactivity); low lipid oxidation genotype (low lipid oxidizer); and adipogenesis genotype (ability to expand the complement of adipocytes and high lipid storage capacity).21 Others have summarized this mismatch between genes and environment as “Stone Age” genes with “Space Age” circumstances.22

Section snippets

Childhood Obesity

Over the span of 4 decades there has been an alarming increase in childhood obesity in both industrialized and developing countries. In general, body mass index (BMI) is the most commonly used metric to classify (over)weight status, given availability of age, gender, height and weight in national datasets, as contrasted to other measures which are not typically available, such as percent body fat and waist circumference. Data from NHANES 2005-2008 reveal an estimated 17% of US children ages

Relationship of Obesity and Timing of Puberty in Boys

Although the literature is consistent regarding the relationship of BMI and timing of puberty in girls, it is not so consistent about this relationship in boys. There are several groups who noted that boys with greater BMI62, 63 or fat mass64 enter puberty earlier. In part, greater BMI may represent adequate caloric reserves rather than obesity; for example, in the study by Boyne et al,64 there was a positive association between body fat and greater pubic hair maturation up to 18 kg body fat,

Conclusion

We have examined the decline in the age of breast development and potential mechanisms to explain the relationship between greater body mass index with earlier puberty in girls. As noted earlier, the epidemiologic studies have documented earlier breast maturation, the typical biologic landmark of pubertal maturation. Several recent investigators have suggested that these changes may reflect pubertal changes rather than reactivation of the hypothalamic-pituitary-ovarian axis, and several

Acknowledgments

The authors wish to acknowledge the cheerful administrative assistance of Lynn Hanrahan.

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    This publication was made possible by the Breast Cancer and the Environment Research Program (BCERP) award numbers U01ES012770, U01ES012771, U01ES012800, U01ES012801, U01ES019435, U01ES019453, U01ES019454, and U01ES019457 from the National Institute of Environmental Health Sciences (NIEHS) and the National Cancer Institute (NCI); P01ES009584 and P30ES006096 from NIEHS; and UL1RR024131, CSTA-UL1RR029887 and CSTA-UL1RR026314 from the National Center for Research Resources (NCRR). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIEHS or NCI, the National Institutes of Health, the Centers for Disease Control and Prevention, or the California Department of Public Health.

    The authors indicate no conflict of interest.

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