Link Between Body Fat and the Timing of Puberty
Total Page:16
File Type:pdf, Size:1020Kb
SUPPLEMENT ARTICLE Link Between Body Fat and the Timing of Puberty Paul B. Kaplowitz, MD, PhD Department of Endocrinology, Children’s National Medical Center, Washington, DC The author has indicated he has no financial relationships relevant to this article to disclose. ABSTRACT Several recent studies suggest that the timing of the onset of puberty in girls has become earlier over the past 30 years, and there is strong evidence that the increasing rates of obesity in children over the same time period is a major factor. This article www.pediatrics.org/cgi/doi/10.1542/ reviews studies from the United States that examined the age of menarche and the peds.2007-1813F age of onset of breast development and pubic hair as a function of body mass index, doi:10.1542/peds.2007-1813F which is a good surrogate measure of body fat. These studies are nearly all cross- Key Words obesity, BMI, menarche, early puberty, sectional, so many questions remain unanswered. However, at least several studies leptin show that girls who have relatively higher body mass index are more likely to have Abbreviations earlier menses, as well as a relationship between body mass index and other mea- NHANES—National Health and Nutrition sures of pubertal onset. The evidence published to date suggests that obesity may be Examination Survey causally related to earlier puberty in girls rather than that earlier puberty causes an DEXA—dual-energy radiograph absorptiometry increase in body fat. In contrast, few studies have found a link between body fat and PROS—Pediatric Research in Office earlier puberty in boys. A growing body of evidence from both rodent and human Settings studies suggests that leptin may be the critical link between body fat and earlier NHES—National Health Examination puberty. Leptin-deficient mice and humans fail to enter puberty unless leptin is Survey GnRH—gonadotropin-releasing hormone administered, and rodent studies indicate that very low levels of leptin stimulate LH—luteinizing hormone gonadotropin secretion both at the hypothalamic and the pituitary level. Current FSH—follicle-stimulating hormone evidence indicates that leptin appears to play a permissive role rather than act as the DHEA-S—dehydroepiandrosterone sulfate critical metabolic signal initiating puberty. The linkage between body fat and the Accepted for publication Sep 5, 2007 reproductive axis in girls may have evolved in mammals as a mechanism for ensuring Address correspondence to Paul B. Kaplowitz, MD, PhD, 111 Michigan Ave NW, Washington, that pregnancy will not occur unless there are adequate fat stores to sustain both the DC 20010. E-mail: [email protected] mother and the growing fetus. PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2008 by the American Academy of Pediatrics HISTORICAL PERSPECTIVES Records from several northern European countries, particularly Norway, Denmark, and Finland, document that the age of menarche, a convenient marker for the timing of puberty in girls, decreased from ϳ16 to 17 years during the 19th century to ϳ13 years by the middle of the 20th century.1 In the United States, a decline from 14.75 years in 1877 to just under 13 years by the period of 1950 to 1970 has been reported. It has been widely assumed that improved health and nutrition associated with the coming of the Industrial Revolution were responsible for most if not all of that decline in the mean age of menarche. At the very least, these historical data suggest that the timing of puberty is not solely genetically determined but can be influenced by epigenetic factors. There have also been studies to suggest that obese girls tend to mature earlier than normal and that “thin” girls tend to mature later. For example, a significant delay in puberty and menarche is seen in girls who are very physically active and have markedly diminished body fat.2 After reviewing longitudinal growth data for 181 normal girls, Frisch and Revelle3 observed that the mean weight at menarche was constant at ϳ48 kg for girls who reached menarche before age 12, between 12 and 13, between 13 and 14, and after age 14; however, mean height at menarche increased progressively the older the girls were at the time of menarche. These observations led Frisch to propose that a critical weight is required to initiate and sustain menses in young girls and that this relationship could explain the secular trend toward earlier menarche during the previous century. One problem with this theory is that although the average weight at menarche in this study varied little with the age at menarche, there was a broad distribution of weights (anywhere between 35 and 60 kg) at the time when individual girls reached menarche. One could interpret the same data as indicating that weight is an important factor but by no means the main determinant of age at menarche. Frisch, relying heavily on studies involving loss of reproductive function in women after weight loss, later modified her theory to suggest that there is a critical fat mass (ϳ17% of body weight) required for menarche and a higher fat mass (22% of body weight) needed for maintenance of reproductive capacity.4 In contrast, Garn et al5 looked at skinfold S208 KAPLOWITZ Downloaded from www.aappublications.org/news by guest on October 6, 2021 TABLE 1 Percentage of 6- to 11-Year-Old Children With a BMI at BMI and fat mass (measured by dual-energy radiograph >95th Percentile absorptiometry [DEXA]) was 0.94 and 0.96 for black and white girls, respectively, and for BMI versus percentage Years of Boys Girls Study body fat, the correlations were 0.83 for both races. The White Black White Black correlations were lower for boys (0.85 and 0.86 for BMI 1963–1965 5.6 2.0 5.1 5.3 versus fat mass and 0.54 and 0.50 for BMI versus per- 1976–1980 7.9 7.9 6.4 11.3 centage body fat). 1988–1991 10.4 13.4 10.2 16.2 The National Heart, Lung, and Blood Institute’s Na- 1999–2000 12.0 17.1 11.6 22.2 tional Growth and Health Study is a cohort study of Based on 4 national surveys spanning 5 decades. 2379 girls divided approximately equally between white Adapted from Troiano RP, Flegal KM, Kuczmarski RJ, Campbell SM, Johnson CL. Arch Pediatr and black girls who were recruited in 1987 at age 9 from Adolesc Med. 1995;149(10):1085–1091 and Ogden CL, Flegal KM, Carroll MD, Johnson CL. JAMA. 2002;288(14):1728–1732. schools in Richmond, California, and Cincinnati, Ohio, and a large group practice in the Washington, DC, area. Each girl was examined yearly for height, weight, skin- fold thickness, and stage of pubertal maturation. A re- thickness of premenarcheal and postmenarcheal girls of cent analysis of this cohort showed that the mean age at the same age and found extensive overlap; he concluded menarche was 12.7 years in white girls and 12.0 years in that there was no clear evidence of a threshold level of black girls. The black and white girls were separated into weight or fatness that is critical for the onset of men- 3 groups according to the age of onset of menarche. arche. Nonetheless, evidence has accumulated in the Across the entire 9- to 18-year age range studied, the past 30 years that points to a major influence of body fat earlier maturing white and black girls had consistently as the timing of puberty, at least in girls. Although the higher BMIs than the midonset girls, who had higher role of environmental chemicals has not been ade- BMIs than the late-onset girls.9 Similar findings were quately studied, the well-documented epidemic of obe- reported when the sum of skinfold thickness was exam- sity in American children provides a plausible explana- ined in relation to the timing of menses; however, there tion for the decreasing age in both the age of onset of was no association between age at menarche and body breast development and the age of menarche. In this fat distribution. review, the studies presented support a link between In 1997, the results of the cross-sectional Pediatric these 2 phenomena. Although there are much fewer Research in Office Settings (PROS) study of female pu- data concerning the possible link of obesity with early berty were published as discussed elsewhere in this sup- puberty in boys, this is reviewed and contrasted with the plement.10,11 For testing of the hypothesis that obesity findings in girls. was a major predictor of earlier puberty in black and white girls, each child between the ages of 6 and 12 had INCREASING PREVALENCE OF OBESITY IN US CHILDREN her BMI calculated and then converted to a BMI SD or z There is ample evidence for the increasing prevalence of score using the tables derived from the NHANES III obesity in all segments of our population, including chil- study.12 The values used were based on the entire sample dren, in the last 30 years. Table 1 compares the preva- of 2200 to 4300 girls per age group, rather than the lence of obesity, defined as a BMI Ͼ95th percentile for slightly different values calculated for black, Hispanic, age and gender, for black and white boys and girls be- and white girls. For example, for 7-year-olds, the mean tween the National Health and Examination Survey BMI was 16.2 Ϯ 2.2; thus, a girl whose BMI was 17.3 (NHANES) study from 1963 to 1965, NHANES II from would have a BMI z score of (17.3 Ϫ 16.2) Ϭ 2.2 ϭ 0.5.