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Kaiser Permanente Study: Maternal Overweight and Hyperglycemia Linked to Early-Onset of Puberty in Girl
Authors: Danielle E. Buttke, Kanta Sircar and Colleen Martin
Buttke, D. E., Sircar, K., & Martin, C. (2012). Exposures to endocrine-disrupting chemicals and age of menarche in adolescent girls in NHANES (2003-2008). Environmental Health Perspectives, 120(11), 1613+. Retrieved from https://ntserver1.wsulibs.wsu.edu:5789/apps/doc/A332379681/OVIC?u=pull21986&sid=OVIC&xid=1235d5c6

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Ethnic Differences in the Presence of Secondary Sex Characteristics and
Menarche Among US Girls

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Factors Affecting Age of Puberty in Girls

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"You are a woman now." Many of us heard those words when we got our first period, a landmark event in a woman's life. It is a day we all remember, sometimes with embarrassment, but it's a subject most women have rarely been able to read about. In the recently released " My Little Red Book," 18-year-old Rachel Kauder Nalebuff broke the unspoken taboo by collecting dozens of essays on the topic from a diverse group of women, both famous and not. Erica Jong writes about the "Fear of Fourteen" and Cecily Von Ziegesar, author of the "Gossip Girl" series, describes an unfortunate sex-ed class on the subject. The collection is just one of a host of new books on the subject; preteens now have dozens of detailed guides to the physical and psychological changes that precede and accompany a girl's first menstrual period. But the mysteries of when and why girls begin puberty have gotten a lot of attention from the scientific community recently, too-research has expanded from the biology of menstruation to include some of the complex sociological and emotional factors involved in when and why girls begin maturing.

Scientists have been particularly puzzled by what appears to be a slight decline in the average age of puberty. The dip isn't much-from two months to a year, depending on the study. No one yet knows why, although there are a number of intriguing theories, nor even whether it's a problem. In the 1960s, says Dr. Paul Kaplowitz, an endocrinologist at Children's National Medical Center in Washington, D.C., girls typically developed breasts and pubic hair between ages 10 and ll. Now, he says, it has fallen to between 10 and 10½. Race also appears to play a role. For example, African-American girls tend to show the first signs of puberty-breast growth and pubic hair-a year earlier than white girls.

Some scientists say they suspect the change is related to the growing numbers of children who are overweight or obese. "That is my preferred theory," says Kaplowitz, author of "Early Puberty in Girls." "There is lots of evidence that where there is an increase in obesity, there's an increase in precocious puberty." The idea is that puberty begins once girls reach a certain weight or body-fat content, so if that point is reached earlier, puberty begins earlier. Fat is also a source of estrogen, so young girls with a lot of body fat would be exposed to more of the hormone.

But while a number of recent studies have found a strong association between early puberty and increased body-mass index (BMI), that link doesn't explain all cases. Kaplowitz notes that girls who are not overweight may still experience puberty earlier than average. In some cases, genetics may offer an explanation: "If a mom had her first period at age 10, 10½, there's a 50 percent chance that her daughter will mature early," Kaplowitz says.

Other scientists think fathers may play a role in some surprising ways. Bruce Ellis, a professor of family studies and human development at the University of Arizona, has been studying the effect of family structure on puberty. He has found that young girls who spent more time living in a home without their birth fathers were more likely to go through puberty early. One explanation might be chemical: animal studies have shown that exposure to the pheromones (chemical triggers) of biological fathers appears to slow down puberty in females. But other factors could be at work as well.

In a study published last year in the journal Developmental Psychology, Ellis and Jacqueline Tither of the University of Canterbury in New Zealand studied sisters in 90 intact families and 70 families where the parents had divorced. The most striking finding concerned sisters in divorced families where the father had engaged in high-risk behavior (defined as a history of violence, depression or imprisonment) and then left home. Younger sisters in those families tended to go through puberty nearly a year earlier than their older sisters, indicating that emotional stress at a certain period early in life may affect a girl's normal development.

As the scientists look for answers, less credible theories abound. A common one blames consumption of bovine growth hormone in cows' milk. "You wouldn't believe how often I am asked that question," says Kaplowitz, "and the answer is no. Even if it is in the milk, it gets chewed up in the digestive tract. Besides, there's no reason to think that bovine growth hormone would have any effect on humans."

And it's still not clear whether entering puberty six months or a year earlier really has any long-term ill effects. Although there is evidence that early menstruation increases the risk of breast cancer because of increased lifetime exposure to estrogen (late menopause has a similar effect), scientists don't know whether starting just a few months earlier makes a difference. "There are many more health consequences to being overweight than having your period at 12 instead of 12½," Kaplowitz says. Early development of breasts and pubic hair can sometimes be a social problem. "It can be a little hard on the girls," Kaplowitz says. "If they are the only ones going through this, they can feel different, and those early periods can be stressful." And for some tweens, having a physical appearance that is more mature than their emotional age can also be a problem when it comes to navigating the world of boys and dating.

When should parents be concerned? Kaplowitz says that any girl who shows signs of puberty before the age of 6 needs to be seen by a specialist. There are no firm rules on girls who start developing at 7 or 8. "You can't just go by age" at that point, he says. Some girls might start getting breasts but then not get periods for a while. "You have to consider the speed at which puberty progresses," he says. "If changes are occurring slowly, we are less concerned."

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Factors Affecting Age of Puberty in Girls

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"You are a woman now." Many of us heard those words when we got our first period, a landmark event in a woman's life. It is a day we all remember, sometimes with embarrassment, but it's a subject most women have rarely been able to read about.

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Puberty is a developmentally plastic phase. Variations in pubertal tempo have implications for the risk of later adult diseases. Influences on pubertal tempo have been widely discussed, but the underlying biological mechanisms remain unclear. Epigenetic modifications are known to regulate development processes; they could play an important role in affecting pubertal outcomes. We conducted a population-based analysis to investigate the association of peripubertal blood DNA methylation at LINE-1 and growth-related candidate genes with pubertal onset and progression in healthy adolescents. The analytic sample included 114 males and 129 females aged 10 to 18 years. DNA methylation at growth-related candidate loci IGF2, H19, HSD11B2, as well as LINE-1 repetitive elements were quantified. Cox survival and ordinal regression models were used to examine sex- and locus-specific associations of epigenetic markers with pubertal development using physician-assessed Tanner stages and self-reported menarche, adjusted for covariates. Among boys, DNA methylation at H19 was associated with later pubarche. HSD11B2 methylation was associated with earlier onset of pubic hair and genitalia development and slower pubertal progression. IGF2 was associated with later onset of genital development. Among girls, LINE-1 methylation was associated with later onset of breast development. For each percent increase of methylation at H19, there was 5% increased odds in the earlier onset of breast development. DNA methylation of IGF2 was associated with earlier onset of pubic hair. DNA methylation at genes known to influence early-life growth may also influence pubertal outcomes.

Additional information

Funding

This work was supported by U.S. Environmental Protection Agency (US EPA) grants RD834800 and RD83543601 and National Institute for Environmental Health Sciences (NIEHS) grants P20 ES018171, P01 ES02284401, R01 ES007821, and P30 ES017885. This study was also supported and partially funded by the National Institute of Public Health/Ministry of Health of Mexico. The contents of this publication are solely the responsibility of the grantee and do not necessarily represent the official views of the US EPA or the NIH. Further, the US EPA does not endorse the purchase of any commercial products or services mentioned in the publication.

Implications and contribution

Our results show that peripubertal blood DNA methylation at growth-related candidate loci IGF2, H19, HSD11B2, as well as LINE-1 repetitive elements may influence pubertal onset and progression. We believe the findings will help to understand and develop future scientific knowledge and potential intervention strategies accommodating the health needs of adolescents.

Acknowledgment

The authors acknowledge the research staff at participating hospitals and the American British Cowdray Hospital in Mexico City for providing research facilities. We thank the mothers and children for participating in the study

Disclosure statement

No potential conflict of interest was reported by the authors.

Supplementary Material

Supplemental data for this article can be accessed here.

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Association of blood leukocyte DNA methylation at LINE-1 and growth-related candidate genes with pubertal onset and progression

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Puberty is a developmentally plastic phase. Variations in pubertal tempo have implications for the risk of later adult diseases. Influences on pubertal tempo have been widely discussed, but the underlying biological mechanisms remain unclear. Epigenetic modifications are known to regulate development processes; they could play an important role in affecting pubertal outcomes.

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Factors influencing that age at which girls begin puberty
https://www.acsh.org/news/2015/02/05/factors-influencing-age-girls-begin-puberty

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Last week, we exposed the flaws of a study published by a group from the Harvard School of Public Health claiming that girls who drink more sugar sweetened soda have their first period a few months earlier than those who don t. ACSH s Dr. Josh Bloom concluded that although this study made for a great headline, the science was lousy. However, according to research done by Dr. Louise Greenspan, a pediatric endocrinologist at Kaiser Permanente, and Dr. Julianna Deardorff, an associate professor in the Maternal and Child Health Program at the University of California, Berkeley, some girls are now starting puberty before the age of 10. They ve been following girls since 2005 and found that by age 7, 23 percent of black girls, 15 percent of Hispanic girls and 10 percent of white girls began to develop breasts.

They point to a number of factors contributing to this phenomenon in an op-ed in the New York Times, some of which we can get behind. The real culprits, they say, are obesity and family stress. We ve written about the link between obesity and the declining age at which girls reach puberty before. And Drs. Greenspan and Deardorff explain the link between increased estrogen secretion as a result of increased body fat, which then leads to earlier breast development. However, they also claim that sugary beverages are the main culprit, at least for the obesity problem, pointing to the study we debunked last week.

Then, of course, endocrine-disrupting chemicals (EDC) are raised as a concern because of their alleged ability to mimic estrogen. However, as we ve pointed out before, the term endocrine disruptor has no real scientific or medical meaning. And, an objective study by several academics with no ties to industry revealed their assessment of EDC risk thusly: Overall, despite of 20 years of research, a human health risk from exposure to low concentrations of exogenous chemical substances with weak hormone-like activities remains an unproven and unlikely hypothesis.

Lastly, they explore the link between early puberty and family stress. Things such as an unpredictable household, the absence of a father in the home and high levels of conflict are associated with a lower age of reaching puberty. They say:To buffer against toxic stress, parents should prioritize setting aside time to engage with their daughters and bond emotionally, but puberty is a complex biological phenomenon that is unlikely to be triggered by a single factor.

ACSH s Ariel Savransky adds, It s clear that there is a link between family relationships and eating habits. Numerous studies have concluded that eating meals as a family can not only improve children s eating habits but also foster a sense of belonging and value for the teen. And eating together is a tangible goal that families can work on. This could be a good place to start, and working on eating habits could then affect weight which can then affect age at which a child enters puberty.

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Factors influencing that age at which girls begin puberty

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Last week, we exposed the flaws of a study published by a group from the Harvard School of Public Health claiming that girls who drink more sugar sweetened soda have their first period a few months earlier than those who don t. ACSH s Dr. Josh Bloom concluded that

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Environmental Factors that Effect Puberty

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Genetic and Environmental Influences on Pubertal Timing Assessed by Height Growth

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Wierenga, Lara M. ; Bos, Marieke G. N. ; Schreuders, Elisabeth ; Kamp, Ferdi V. D. ; Peper, Jiska S. ; Tamnes, Christian K. ; Crone, Eveline A.

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The relationship between obesity and body compositions with respect to the timing of puberty in Chongqing adolescents: a cross-sectional study

He, Fang, et al. “The Relationship between Obesity and Body Compositions with Respect to the Timing of Puberty in Chongqing Adolescents: a Cross-Sectional Study.” BMC Public Health, BioMed Central, 18 Aug. 2017, www.ncbi.nlm.nih.gov/pmc/articles/PMC5563015/.

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Abstract

Background

It is well known that excess adiposity during childhood may influence pubertal development. However, the extent to which body compositions vary in throughout puberty in boys and girls is currently unknown. The aim of this study was to investigate whether obesity and body compositions correlate with the timing of puberty in boys and girls.

Methods

By random cluster sampling, our study analyzed data from 1472 students (690 girls, 782 boys) aged 6-17 years from two schools in the Chongqing area. Data were collected by physical examination of weight, height, and skinfold thicknesses. Testicular volume was measured in boys and breast development in girls. By which we got the indicators of obesity, timing of puberty and body compositions. Probit regression analysis was used to group subjects into early puberty (>P ₂₅), on-time puberty (P ₂₅ ~ P ₇₅), and delayed puberty (<P ₇₅). Chi-square test was applied to assess the distribution differences of fat levels among puberty groups by sex. Multivariate analysis of covariance was used to examine the association between timing of puberty and body composition indicators.

Results

There were significant differences in the distribution of fat levels (normal weigh, overweight, obesity) among different pubertal groups in different sex (boys: χ2 = 10.639, P = 0.031; girls: χ2 = 63.232, P = 0.000). Multivariate analysis of covariance showed that percentage of body fat, fat mass and fat-free mass in the delayed puberty girls were significantly lower than the girls in the on-time puberty and early puberty, while body density had the opposite result (all P < 0.001). Body density, percentage of body fat, fat mass and fat-free mass of boys all had no significant difference among different timing of puberty groups (all P > 0.05).

Conclusions

In girls, delayed puberty was negatively correlated with Obesity, percentage of body fat, fat mass and fat-free mass, and positively correlated with body density. But in boys, delayed puberty was only negatively correlated with Obesity, the relation between puberty and body compositions was not found.

Keywords: Obesity, Body compositions, Timing of puberty, Adolescents

Background

Puberty represents a period during development of gradual transition from childhood to adulthood. The WHO Expert Committee states that adolescent ages range from 10 to 20 years old. However, there are significant differences in the age of onset, speed of development and age of maturity. Studies have found that the onset and development of puberty are primarily controlled by the interaction between genetic and environmental factors. At present, there is no consensus on the mechanism for initiation of puberty, but the more widely accepted view is that the central nervous system, particularly the hypothalamic-pituitary-gonadal (HPG) axis, plays a decisive role [ 1].

Early puberty is defined as the appearance of adrenocortical function, gonad function, and menarche earlier than the first quartile of the age distribution in children [ 2], and this phenomenon has received increasing attention during the past couple of decades. Some studies have found that girls who experience an earlier menarche age were taller in early adolescence but shorter in early adulthood than those who matured later, despite having a greater peak height velocity and greater post-menarche increase in height [ 3].

In recent decades, the prevalence of childhood and adolescent obesity has been rapidly increasing and has become a major public health concern both in China and worldwide. Studies have shown that obesity is associated with earlier puberty onset among adolescent girls and young female adults [ 4- 7]. For instance, girls who had more body fat content were more likely to experience menarche at younger ages [ 8] and early maturing adolescent girls were almost twice as likely to be overweight than average-maturing girls [ 9]. In boys, however, some research has suggested that early-maturing boys were less likely to be obese compared to boys who matured at the average rate [ 4].

In the majority of studies, obesity is defined by Body Mass Index (BMI) level; however, this metric is not entirely suitable for children [ 10], and the sensitivity of using BMI to identify children with obesity was generally only low to moderate [ 11, 12]. As early as 400 BC, the Greeks put forward the concept of body composition [ 13]. Behnke et al. [ 14] divided body composition into fat mass (FM) and fat-free mass (FFM) and found that the proportion of body compositions between males and females is different. Burton RF [ 15] found that the relationships between FFM and FM were linear and FM were correlate with height. But the interrelationships among FM, FFM, total body mass (BM) and height have long been studied in relation to the BMI [ 16, 17]. Although BMI (kg/m ²) is widely used as a measure of adiposity, it is a measure of excess weight relative to height (overweight) rather than excess adiposity (obesity) [ 18]. A study of 2554 school children found a correlation of r = 0.58 between BMI and body fatness (assessed by skinfolds) among boys who were relatively fat, but no association ( r = 0.01) among leaner boys [ 19]. Norgan NG et al. [ 20] found that the relationships between BMI and body compositions differed with age, sex, and ethnicity and body shape. Moreover, recent study reported that skinfold thickness during childhood and adolescence is a better predictor of high body fatness in adults than BMI [ 21]. Moreover, changes in skinfold thickness or in percentage body fat have been considered more precise than BMI to monitor obesity, thus providing greater confidence for epidemiological applications. Therefore, the assessment of obesity should ideally be based on measurement of body compositions [ 22].

This study assessed whether obesity correlates to timing of puberty, specifically determining whether higher skinfold thickness, percentage of body fat (%BF), FM and FFM associate with early puberty. More importantly, a comprehensive examination of the association in boys and girls between early puberty and obesity incidence provides useful insights to advance our understanding of the relationship between these phenomena.

Methods

Study sites and subjects

This survey was a cross-sectional study. A three-stage random cluster sampling method was used in this survey. In stage one, a central district was chosen in Chongqing. In stage two, two nine-year schools, with grades one to six belonging to primary school and grades seven to nine belonging to junior middle school, were chosen. One of the schools was located in an urban area, while the other was in a village. Students in these two schools represented both high and low levels of economic development. In the third stage of sampling, girls from grades two and three and boys from grades three and four were selected from each school; simultaneously, both girls and boys in grades seven and eight were selected. Three to five classes were selected from each grade. The grades this study chose to examine mostly encompass all the early and delayed individuals with respect to puberty development. Girls from grade two and boys from grade three were chosen due to the difference in onset of early puberty, being approximately seven years old in girls and about eight years old in boys.

A total sample of 1472 students (690 girls, 782 boys) aged 7 to 17 years were selected in this survey. All individuals completed a physical examination. The study was approved by the ethic committee of Chongqing Medical University. Written informed consent was also obtained from a parent or guardian on behalf of each child.

Data collection

This study mainly based on a physical examination, including weight, height, tricep skinfold thickness, subscapular skinfold thickness and suprailiac skinfold thickness. At the same time, breast development in girls, and testis volume in boys, were examined. The evaluation methodology of these indicators was as follows:

Pubertal Assessment

Breast stages (stage 1-5) were assessed by visual inspection and palpation using the rating scales of Marshall and Tanner [ 23]. The volume of each testis was estimated by comparative palpation with an orchidometer. To classify boys puberty status, volume of testis (VOT) were divided into 4 stages: stageI,VOT < 4 ml; stageII, 4 ml ≤ VOT < 12 ml; stage III, 12 ml ≤ VOT < 20 ml; stage IV, VOT ≥ 20 ml. Median ages at breast stage 2 and 4 ml of VOT are considered the beginning of puberty for our use [ 24, 25]. Subjects were grouped using the quartiles of the decimal age adjusted for Tanner stages of puberty and gender. For example, in Tanner stage 1, children and adolescents were considered as 'in early puberty' if they were in the first quartile of the decimal age for that stage and gender. The same procedure was used for all the other Tanner stages. Those in the fourth quartile of the decimal age are considered as 'those with delayed puberty', and if they were between first and fourth quartile of the decimal age, they are considered to be 'on-time' [ 6]. It is worth noting that girls who were in breast 1 and boys whose VOT < 4 ml were regarded as 'not having begun puberty', and were not included in later analyses. The formula used to calculate the decimal age of P ₂₅, P ₇₅ for each stage are as follows: Probit (P) = α + Σßx.

Anthropometry

Measurements of weight, height and skinfold thickness were collected from all subjects. Standing height was measured to the nearest 0.1 cm using a height meter. Weight was measured on a digital electronic scale with a precision of 0.1 kg. The children were weighed without shoes, wearing light clothing. Skinfold thickness was taken with a Harpendencalliper on the right side of the body with a precision of 0.1 mm. We calculated BMI (= weight [kg]/height[m] ²) and the sum of skinfold thickness (SST) (= triceps skinfold thickness + subscapular skinfold thickness) for each individual as well. It is worth noting that the final values of skinfold thickness should be only half of the measured results, as we measured the double skin fold. All surveyors received standardized training before this survey.

Definition of Obesity and Overweight

To define obesity and overweight, children aged 7-18 years were categorized according to sex-age-specific BMI cut offs recommended by the Chinese Working Group on Obesity (WGOC) [ 26].

Body Compositions

Firstly, SST was used to calculate Body Density (BD). BD formulas are shown as follows [ 1]: BD = 1.0879-0.0015 × SST for both7-11 years boys and girls; BD = 1.0868-0.00133 × SST for 12-14 years boys, BD = 1.0888-0.00153 × SST for 12-14 years girls; BD = 1.0977-0.00146 × SST for 15-18 years boys, BD = 1.0931-0.0060*SST for 15-18yearsgirls. Next, we used the following formula to calculate %BF with BD: %BF = (4.57/BD-4.142) × 100. Finally, FM and FFM were used as additional measures of body composition according to Maynard et al. [ 10]: FM = weight × %BF and FFM = weight - FM.

Data analysis

Using the probit regression analysis, we calculated the quartiles of the decimal age of each Tanner stage for girls' breast and boys' testis, by which subjects were grouped into early puberty (>P ₂₅), on-time puberty (P ₂₅ ~ P ₇₅), and delayed puberty (<P ₇₅). Chi-square test was used to explore whether there were differences between boys' and girls' timing of puberty, and compared the distribution difference of fat levels between pubertal groups by sex. Finally, BD, %BF, FM and FFM as the independent variable, pubertal groups (early puberty, on-time puberty and delayed puberty) as dependent variable, multivariate analysis of covariance were used to examine whether body compositions varied with respect to different pubertal groups. Data management and data analysis were performed with SPSS Version 19.0. Any result with a P-value less than 0.05 was considered statistically significant. When compared the difference in each obesity and body composition measure by 3 groups of puberty timing, Chi-square test and multivariate analysis of covariance sufficed with correction of p-values.

Results

Characteristics

Table presents the characteristics of the study sample, including mean age, the number of different school and grade, anthropometric and body compositions grouped by sex.

Table 1

As shown in Tables , 441 boys and 407 girls had entered puberty. By using the probit analysis to calculate the quartiles of the decimal age of each Tanner stage for girls' breast and boys' testis, the subjects were grouped into three groups: early puberty, on-time puberty, and delayed puberty. Over one eighth of the boys (12.7%) were classified as early puberty, nearly three quarters of boys (70.3%) were on-time puberty, and 17.0% were regarded as experiencing delayed puberty. Approximately one fifth of girls (19.7%) were experiencing early puberty, 38.0% of girls developed on-time, and 42.3% of girls were developing later than others. The percent of early and delayed puberty girls was significantly higher than boys ( P = 0.007, P < 0.001, separetely), and the percent of on-time puberty girls was significantly lower than boys ( P < 0.001).

Table 2

Association between obesity, overweight and puberty timing

The prevalence of obesity and overweight in boys and girls in different pubertal groups were presented in Table . There were significant differences in the distribution of fat levels (normal weigh, overweight, obesity) among different pubertal groups in different sex (boys: χ2 = 10.639, P = 0.031,girls: χ2 = 63.232, P = 0.000).

Table 3

Body compositions compared to timing of puberty

As shown in Table , BD, %BF, FM and FFM of boys had no significant difference among different timing of puberty group (all P > 0.05). But all indicators in the delayed puberty were significantly lower than in the on-time puberty and the early puberty girls, except for BD had the opposite result (all P < 0.017).

Table 4

Discussion

This study examined how children's fat levels (obesity and overweight) and body compositions varied with respect to timing of puberty development based on the evaluation of breast development in girls and the volume of each testis in boys according to the Tanner stage standard.

Although the mechanism of association between obesity and early puberty in girls remains to be elucidated, the relationship between obesity and early puberty are consistent. Obesity and overweight are positively correlated with early puberty [ 4- 7, 27, 28]. This study also found that there were significant differences in the distribution of overweight and obesity among the groups of early puberty, on-time puberty, and delayed puberty.

In boys, the relationship is still controversial. Wang [ 4] examined the influence of early sexual maturation on fat in 1520 US boys aged 8-14 years and found that early sexual maturation was negatively correlated with obesity. However, Lee et al. [ 29] reported the opposite in 705 American boys. In Chinese boys, the relationship seems to be positive [ 30]. In this study, the rates of overweight and obesity in delayed puberty group were significantly lower than that in on-time and early puberty group. This result was consisted with J. Ribeiro's research [ 6] but contrary to Wang's [ 4] and Fang Qi's [ 28]. These disparities could be due to differences in age structure between the studies or the use of variable criteria for judging puberty timing. In addition, for different social and cultural adolescents, eating habits and nutritional status are different, which may also affect the growth and development of boys [ 31].

Bao et al. [ 32] reviewed various recent studies that examined the relationship between overweight/obesity, body compositions and puberty events in females and concluded that higher BMI and body fat content before or during puberty can accelerate the onset of puberty. Remer et al. [ 33] found that increased body fat may be important for the secretion of androgens in girls. Blank et al. [ 34] believe that the high concentration of androgens in obese girls may promote increased secretion of GnRH, resulting in early puberty. A study by Brill in rodents found that high fat diets lead to rat vaginal opening in advance and that blocking the androgen receptor can reverse this phenomenon [ 35]. These observations may explain the effect of body fat on puberty that we observed in this study, as we also found in girls that FM in delayed puberty group was significantly lower than that in on-time puberty group or early puberty group. In addition, we also found that the FFM in the delayed puberty group was significantly lower than that in the early puberty group and the on-time puberty group, while BD in the delayed puberty group was significantly higher than that in the early puberty group and the on-time puberty group. These indicated that girls who have low body mass and weight, high BD, could have a delayed puberty. But the FM, FFM, and BD of boys were not significantly related to their timing of puberty. There was no significant difference in body fat and body weight between boys and girls in childhood, but with age, especially after puberty, %BF of boys and girls showed significant difference [ 36]. Under the influence of sex hormone, the muscle and bone of boys developed rapidly, lead to FFM increased significantly and %BF of boys decreased significantly, while the %BF of girls increased significantly. What's more, the amount of exercise of boys was usually higher than that of girls, and exercise can increase lean body mass and decrease body fat. Data showed that %BF of 18 years old Chinese boys (17%) was significantly lower than that of Chinese girls (27.8%) [ 1]. In the whole process of growth and development, the level of serum leptin has great changes. The level of leptin regulated by many factors in the body, in which, the content of adipose tissue is a major factor, the higher fat content, the higher the level of leptin, and leptin have direct or indirect effects on puberty and reproductive regulation [ 37], which regulates the release of luteinizing hormone releasing hormone (LHRH) in adults, thus directly influences the ovaries and plays an important role in initiation and progression of puberty.

Besides, change of body fat composition and pubertal stages involve extremely complicated genetic and other endocrine processes, and that a final conclusion about the causality between obesity and pubertal development has not been reached in either domestic or international research. The association between puberty onset and development and body fat compositions presented in our survey and others serves as an alert to the importance of considering precocious puberty when looking at high %BF. Ultimately, it is important to remember that these variables are not acting in a vacuum and that other factors should also be considered. Considering socioeconomic status and other potential mediators of puberty may help us to understand the short- and long-term consequences of puberty development with respect to body fat composition and aid in establishing a causal link between them.

Study strengths and weaknesses

Earlier studies have linked early puberty to higher body fat, at least in girls. However, in most large-scale epidemiologic studies, fat mass has not been directly measured. Usually, BMI is used as a surrogate for body fat. Studies found that no matter for white or black girls, the mean BMI z scores of girls with breast development were significantly greater than for age-matched girls who were prepubertal [ 38]. There were positive relations between increasing stages of breast development and BMI, waist circumference, fat mass and %BF [ 39]. However the breast development was assessed by inspection and not palpation, which can cause confusion in overweight girls, in whom fat can mimic breast tissue. As for boys, the relation between body fat and puberty has been controversial. Wang even pointed to the possibility that obesity may actually result in later rather than earlier puberty in boys [ 4]. In this study, we used the breast in girls and testicular volume in boys as the indicator of pubertal timing, and analysed the relation with fat level, which was classified by BMI, and body compositions respectively. We found that the relations were difference. In boys, the rates of overweight and obesity in early puberty group were significant higher than on-time and delayed puberty group. While the relations between pubertal timing and indicators of body composition didn't find. In girls, early puberty was positively correlated with obesity, but the body compositions in early puberty had no statistical difference compared with on-time puberty. These indicate that BMI as a surrogate for body fat can chang the real relation between body fat and puberty. Besides, we found that the development of boys' testicles may not be related to body compositions, but girls' breast development is not only related to FM, but also to FFM. Girl with lighter weight and higher BD could has later breast development.

Some limitations of the present study still should be noted. First, this is a cross-sectional survey, so causal relationships between variables of interest cannot be assessed. Furthermore, the study populations were only based on two schools in one district of Chongqing. Cohort studies with larger sample size and covering wider age range are still needed.

Conclusion

In summary, obesity and overweight are negatively correlated with delayed puberty in girls. Body compositions, such as %BF, FM and FFM are negatively correlated with delayed puberty and BD are positively correlated with delayed puberty in girls. But the relation between obesity or body compositions with timing of puberty was not found in boys. Prospective cohort studies are needed to determine the causality of timing of puberty and obesity and also whether the association between body compositions and timing of puberty merit further attention.

Acknowledgements

We would like to acknowledge the primary and secondary school health care of the Jiu Longpo district for their efforts in helping us communicate with project schools. We are also grateful to Anhui Medical University for providing us with this valuable opportunity.

Funding

This study was supported by National Natural Science Foundation of China (Grant No 81302449).

Availability of data and materials

The datasets collected and/or analyzed during the current study are available from the corresponding authors upon reasonable request.

Abbreviations

Authors' contributions

Conceived and designed the survey: HW; Performed the survey: PG, FH, LP; Analyzed the data: FH, PG; Wrote the paper: FH, PG; Literature review: FH, PG, LP; Interpreted the data and revised the paper: QL, DC. All authors read and approved the final manuscript.

Notes

Authors' information

FH is a master student at School of Public Health and Management, Chongqing Medical University. PG(MS) is a member of Chongqing Health Information Center and a master student at School of Public Health and Management, Chongqing Medical University. QL(PhD) is a professor at School of Public Health and Management, Chongqing Medical University and a visiting scholar at Duke Global Health Institute, Duke University. DC(PhD) is the Research Program Leader at Duke Office of Clinical Research, School of Medicine, Duke University Medical Center. LP is a master student at School of Public Health and Management, Chongqing Medical University. WH(MS) is a professor at School of Public Health and Management, Chongqing Medical University.

Ethics approval and consent to participate

Ethics approval was gained from ethical committee of the Chongqing Medical University. Written consent was obtained for school, teacher, parent and child participation. Parents provided written consent on behalf of children and additional verbal assent was sought from children at the time of data collection.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

References

1. Ji Chengye. child and adolescent health. No. seven. Beijing: People's Medical Publishing House, 2013. p. 27-96.

18. Freedman DS1, Ogden CL, Berenson GS, Horlick M. Body mass index and body fatness in childhood. Curr Opin Clin Nutr Metab Care, 2005, 8(6): 618-623. [ PubMed]

26. Group of China Obesity Task Force, Chengye J. Body mass index reference norm for screening overweight and obesity in Chinese children and adolescents (in Chinese). Chin J Epidemiol, 2004, 25: 97-102. [ PubMed]

36. Freedman DS, Sherry B. the validity of BMI as an indicator of body fatness and risk among children. Pediatrics, 2009, 124 Suppl 1: S23-S34. [ PubMed]

# data[].attributes.attachment_link.title
The relationship between obesity and body compositions with respect to the timing of puberty in Chongqing adolescents: a cross-sectional study

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It is well known that excess adiposity during childhood may influence pubertal development. However, the extent to which body compositions vary in throughout puberty in boys and girls is currently unknown. The aim of this study was to investigate whether ...

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Psychological Factors and Precocious Puberty in Girls
Rebecca Fraser-Thill

Fraser-Thill, R. (2019, January 4). How Stress and Family Dynamics May Lead to Early Puberty in Girls. Retrieved from https://www.verywellfamily.com/precocious-puberty-psychology-3288353

# data[].attributes.attachment_link.readable_text
For girls, precocious puberty (early puberty) is defined as the onset of puberty before 8 years old. Rather than starting at the average age of 10 or 11, some girls have started developing breasts and showing other signs of maturity as early as 5.

Quite often, the exact cause cannot be identified, though biological factors tend to be the primary reasons doctors point to. However, researchers have also found that a number of psychological or psychosocial factors may contribute to a girl experiencing puberty early as well.

Overall, girls today may be experiencing puberty earlier than girls did in the past. It is a phenomenon called the secular trend, which is used to examine decreasing puberty ages since the 1900s. It is an area of study that is of great interest to medical doctors, psychologists, and researchers alike.

If puberty begins too early, though, girls are likely to grow shorter than their peers and face social and emotional problems. For instance, sometimes the changes can be overwhelming for a younger girl if she's not prepared for the transition. It's also common for girls to face stressors caused by their peers if they develop earlier than most of their friends or classmates.

A young girl may be at higher risk for precocious puberty due to a number of factors. On the biological side, doctors often look at things like hormones, genetics, and obesity. For instance, things like meat with a high amount of injected hormones have been blamed for some of the youngest cases.

According to the Mayo Clinic, girls who are overweight or exposed to hormone-containing creams or ointments-including sex creams, medications, and some dietary supplements-are at higher risk. There is also an indication that the brain and pituitary gland of some girls may begin producing and releasing gonadotropin-releasing hormone (Gn-RH) earlier. Additionally, young African-American girls and those with certain medical conditions-including some involving increased production of hormones-are more prone to precocious puberty.

Adding to these possible medical reasons, some studies have pointed to psychological stressors and family influence that may induce puberty at a younger than normal age. These are not a predictor that it will happen, though some evidence has shown that it can increase the risk.

Studies have shown that if a girl doesn't have her biological father living with her, she is likely to reach puberty earlier than girls who have their father present. Some of the findings suggest that the longer dad has been absent, the sooner puberty will begin.

Some researchers believe the presence of a stepfather or mother's boyfriend in the house is even more important to precocious puberty than a biological dad's absence. It is theorized that unrelated males create pheromones-odorless airborne chemicals-that may affect hormonal functioning. These pheromones might cause a girl to develop more quickly.

In other words, it doesn't matter if dad is gone, but rather whether someone has taken his place. This theory has been supported in animal studies, and there is some evidence of it in humans, as well.

There is also the theory that the more a family fights, the earlier a girl in that family is likely to reach puberty. One study, for example, found a correlation between both parents' dissatisfaction within a marriage-particularly a father's withdrawal-and a girl's early development.

Although researchers are not quite sure why this occurs, prolonged stress of any kind-physical, social, or psychological-seems to speed up girls' maturation. Therefore, the conflict between parental figures (whether married or not), dysfunction in the family as a whole, and less warmth in a family have all been found to be related to precocious puberty in girls.

If a parent-particularly the mother-has a mental disorder, there is some evidence that her daughter is likely to have earlier puberty than her peers who have a mentally healthy mom.

Why might the mental health status of a parent matter? Like family conflict, having a parent with a mental disorder can be a source of intense, chronic stress. If stress causes faster maturation, it follows that parental mental health could indeed affect the timing of puberty in a child.

Though you may think that early puberty is just a biological change, it can have negative consequences on a young girl's social and emotional health. If your daughter is experiencing this, it's a good idea to seek professional help. Her medical doctor is a good place to begin finding the support she needs to ease the transition and address any potential issues.

# data[].attributes.attachment_link.title
How Stress and Family Dynamics May Lead to Early Puberty in Girls

# data[].attributes.attachment_link.description
For girls, precocious puberty (early puberty) is defined as the onset of puberty before 8 years old. Rather than starting at the average age of 10 or 11, some girls have started developing breasts and showing other signs of maturity as early as 5.

# data[].attributes.body
Association of prenatal and childhood PBDE exposure with timing of puberty in boys and girls
Kim G. Harley et al.
Harley, K. G., Rauch, S. A., Chevrier, J., Kogut, J., Parra, K. L., Trujillo, C., . . . Lustig, R. H. (2017). Association of prenatal and childhood PBDE exposure with timing of puberty in boys and girls. Environment International,100(2017), 132-138.

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Associations Between Maternal Obesity and Pregnancy Hyperglycemia and Timing of Puberty Onset in Adolescent Girls: A Population-Based Study
Kubo, A., Deardorff, J., Laurent, C. A., Ferrara, A., Greenspan, L. C., Quesenberry, C. P., & Kushi, L. H. (2018). American Journal of Epidemiology, 187(7), 1362–1369. https://doi.org/10.1093/aje/kwy040

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Kylend Woods-Gibson
Relationships between weight and timing of puberty

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Abstract

Menarche is a milestone in a woman's life as it denotes the start of reproductive capacity. Aim of this report is to review the recent developments and the current knowledge in the neuroendocrinology of pubertal onset and the factors, genetic and environmental, that influence menarcheal age. We also review the implications of early or late menarcheal age on a young woman's life.

Background

The landmarks of the pubertal events in girls are the onset of puberty, peak height velocity (PHV) and menarche. The onset of puberty is marked by the development of breast tissue, while PHV is the highest velocity that is observed during the pubertal growth spurt.

Menarche is a rather late event in puberty and usually occurs 6 months after PHV is achieved. The age that menarche occurs varies and is dependent on the interaction between genetic and environmental factors.

In the 19th century factors that were thought to exert an influence on the physical maturation of girls were climate (particularly the mean annual temperature), ethnic origin, social status, urban or rural residence, physical activity, education, sexual stimulation, housing, inheritance, and health status [ 1]. Studies carried out in the 20th century documented other factors associated with the age at menarche, e.g. season and month at birth, physique, position at the sibship, family income, occupation and education of parents and family size [ 1].

It is considered that during the 20 th century the dramatic improvement of socioeconomic conditions and general health of the populations in the industrialized countries resulted in an earlier onset of puberty in children. The most reliable marker of the positive secular changes in pubertal development was the fall of the age at menarche. It has been estimated that during most of the 20 th century age at menarche has been falling by about 3 months per decade [ 2], although there are reports from industrialized countries that it has been leveling off or that it shows an upward trend [ 3, 4].

Whatever the factors that influence pubertal maturation and age at menarche are, they interrelate and thus the onset of menarche cannot be attributed to a single factor.

Aim of this report is to review the neuroendocrinology of pubertal onset and the factors, genetic and environmental, that influence menarcheal age, and also the implications of early or late menarcheal age on a young woman's life.

We searched PubMed for relevant articles, especially published the last decade.

Neuroendocrinology of puberty

Onset of puberty occurs after reactivation of the hypothalamic Gonadotropin Releasing Hormone (GnRH) secretory system. The GnRH secretory network initially develops and is temporarily active during fetal and neonatal life and early infancy, i.e. during the first 6 months of life, the so-called 'mini-puberty'. These early periods of GnRH activation may be important for masculinisation or feminisation of the brain [ 5].

At puberty the pulsatile GnRH secretion, and the subsequent episodic pituitary gonadotropin secretion, which is necessary for normal gonadal development and function, is triggered by the activation of the GnRH pulse generator. GnRH pulse generator is comprised by scattered neurons that are distributed in the arcuate nucleus of the medial basal hypothalamus and the preoptic area in the rostral region of the hypothalamus [ 6]. The GnRH pulsatile secretion is dependent on the coordinated action of the scattered GnRH neurons. The latter are controlled by trans-synaptic, stimulatory and inhibitory, and glia-to-neuron inputs. Various neuropeptides and neurotransmitters have been shown to have stimulatory (e.g. gluatamate, noradrenaline) or inhibitory (e.g. γ-aminobutyric acid-GABA, endogenous opiates, NPY) [ 7] role in the regulation of GnRH neurons (Figure ). The upstream genes involved in the transcriptional control of these components at the time of puberty remain to be identified. Recently, it has been established that glia-to-neuron signals include transforming growth factor-α, neuregulin and glutamergic inputs. GnRH receptors are expressed in the hypothalamic GnRH neurons suggesting that GnRH exerts an autocrine action [ 6, 8].

Studies in human subjects with hypogonadotropic hypogonadism (HH) have disclosed a number of genes that are necessary for normal reproductive function. Among them Kiss1 gene, that produces Kisspeptin, and its receptor, G Protein Coupled Receptor 54 (GPR54) or Kiss1r have emerged as key players in the regulation of reproduction. Neurons that express Kiss1 are distributed within hypothalamus predominantly in the infundibular nucleus and scattered in the medial preoptic area [ 9]. Expression of Kiss1r transcript has been reported in human placenta, pituitary, spinal cord, and pancreas, as well as in other tissues (such as various brain regions, stomach, small intestine, etc) [ 10]. Kisspeptin and GPR54 are expressed in hypothalamic GnRH neurons, suggesting that both GnRHR and GPR54 may act as paracrine and/or autocrine regulators of GnRH neuronal function [ 11]. However, Ramaswamy et al reported that, in primates, kisspeptin-beaded axons, surprisingly, made only infrequent contacts with GnRH neurons in the mediobasal hypothalamus, whereas, kisspeptin and GnRH axons were found in extensive and intimate association in the median eminence indicating that nonsynaptic communication at the level of the median eminence is a pathway contributing to the regulation of GnRH release by kisspeptin [ 12]. It is evident that the hypothalamic kiss-1 system transmits metabolic information to gonadotropic axis, as expression of kiss-1 gene at the hypothalamus is down-regulated in conditions of negative energy balance [ 13]. Thus, GnRH neurons activation by kisspeptin is essential for the onset of puberty and there are data from mice that the activation of kisspeptin neurons are driven by circulating estradiol [ 14].

Studies of families with idiopathic HH pointed to a mutation in GPR54 indicating that this receptor is essential for normal GnRH secretion and pubertal development in the human [ 15]. Recently, an activating mutation of GPR54 was reported as causative of central precocious puberty in a girl [ 16]. It has been for more than a decade now that leptin, a hormone produced by the adipose cells, was established as exerting permissive actions on the onset of puberty by modulating GnRH neurons [ 17], however, the hormone is not able to initiate puberty by itself. Serum leptin levels rise in both sexes at the start of puberty. The important role of leptin in the onset of puberty is highlighted by the fact that children with Leptin gene mutations are markedly obese and delayed in puberty. Leptin is involved in the metabolic regulation of Kiss-1 as it was demonstrated that kisspeptin neurons express leptin receptors [ 18].

Most recently it was shown that central activation of mammalian target of rapamycin (mTOR), a serine/threonine kinase that operates as sensor of cellular energy status, stimulated LH secretion in pubertal female rats via modulation of hypothalamic KiSS-1, whereas mTOR blockade by rapamycin inhibited gonadotropic axis suggesting that central mTOR signaling has a role in the control of puberty onset and gonadotropin secretion [ 19].

For many years, the prepubertal quiescent period is considered to occur due to a high sensitivity of GnRH neurons (gonadostat) to the very low levels of sex steroids and to intrinsic inhibitory mechanisms within CNS that exert a blockade to the hypothalamic GnRH secretion. According to the "gonadostat " theory, the low levels of testosterone/estradiol released by the prepubertal testes/ovaries exert negative feedback effects that inhibit GnRH secretion [ 20]. The major inhibitory factor for GnRH release before puberty, at least in primates, appears to be γ-aminobutyric acid (GABA); the reduction in tonic GABA inhibition results in increase in the release of neurotransmitters, such as glutamate, which is followed by increase in pubertal GnRH release.

In view of the recent study that demonstrated that estradiol is essential for the emergence of kisspeptin expression in GnRH neurons in the prepubertal period, it was proposed that the gradual development of an estradiol-kisspeptin positive feedback relationship provides a GnRH neuron amplification mechanism that is used to facilitate the emergence of pulsatile gonadotropin secretion necessary for puberty onset.

Assessment of menarcheal age

There are three methods for assessing age at menarche, a) the status quo, b) the recall or retrospective, and c) the prospective methods [ 21]. In the status quo method data regarding menarcheal age can be obtained by asking a girl (or her parent) of her "current status", i.e. whether she has had her first menses by the time of assessment, and her birth date. In the status quo method the sample must be large, representative of the population, and in the developed countries the age range should be from 8 to 16 years old.

In the recall method menarcheal data are obtained by asking post-menarcheal females (or their mothers) to recall their age at first menses. The recall method may be less valid and its accuracy is decreased with greater time elapsed between menarche and asking for the date, because it is fraud with poor memory. Furthermore, all girls included must be at an age that they normally should have already started menstruating.

The prospective method is more accurate, however such studies are not easy to perform as they should be longitudinal having premenarcheal girls followed regularly, ideally every 3 months, and asked at each visit whether they have begun to menstruate. Therefore, most studies on menarcheal age have employed the status quo or the recall methods.

There are numerous studies (Table ) examining the secular trend of age at menarche in various populations. In general, there is a continuous trend for earlier ages at menarche for the most part of the 20 th century, although this trend tends to slow down or stabilize. In the United States, the mean age at menarche was more than 14 years prior to 1900 [ 22] and it decreased to 12.43 years in a study conducted between 1988 and 1994 [ 23], although there were significant racial differences in maturational timing. In the Fels Longitudinal Study girls born in 1980 had menarche at 12.34 years of age suggesting a further decrease in menarcheal age [ 24]. Euling et al assessed the data for evidence of a still existing secular trend in puberty timing for data collected from 1940 to 1994 in US girls [ 25]. These data suggest a trend towards an earlier onset of breast development and menarche but not for other female pubertal markers.

Table 1

Maturational tempo differences and age at menarche

A question that arises is what is the association between timing of onset of puberty and menarche, in other words will girls with early puberty invariably have menarche at an early age and vice versa? Data gathered from women born between 1977 and 1979, showed only a moderate correlation between menarche and onset of puberty (.37-.38), whereas in earlier studies conducted on women born between 1920 and the 1960s much higher correlations (.64-.86) were reported [ 26]. This may be explained by a change in the maturational tempo in girls born after the 1970s. Indeed, studies carried out during the last 10 years in Spain, the USA and Greece [ 27- 29] showed that early maturing girls present a compensatory delay in pubertal progression that could explain the moderate correlation between the age at menarche and at pubertal onset.

These studies have shown that early pubertal maturation in girls is associated with a greater pubertal height gain and a longer period of pubertal growth, which is due to a longer pubertal growth up to the stage of peak height velocity, whereas after that stage there is no significant difference to the duration of pubertal growth irrespective of the timing of the onset of puberty [ 29].

Genetic determinants of menarche

Menarcheal age is influenced by heredity but the specific genetic determinants are largely unknown. Evidence for hereditary influences on the age at menarche comes from studies that show a trend for maternal age at menarche to predict daughter's age at menarche [ 30]. In fact, approximately half of the phenotypic variation among girls from developed countries in the timing of menarche is due to genetic factors [ 31].

In search for specific genes determining the timing of menarche Stavrou et al [ 32] evaluated whether the XbaI and PvuII polymorphisms of estrogen receptor a ( ERa) gene are associated with the age at menarche. After adjusting for body mass index this cohort demonstrated that the difference between XX homozygotes and other subjects was 0.57 years (p = 0.021). The difference between PP homozygotes and other subjects was not significant (0.26 years, p = 0.26), while the difference between PX homozygotes and other subjects was 0.67 years (p- = 0.008), suggesting that XbaI XX homozygotes or, in more general terms, subjects homozygotes for the PX haplotype seem to have a modest delay in the age of menarche. Regardless of the exact mechanism, if ERa gene polymorphisms can alter the estrogenic biological activity at the cellular level, this may influence the maturation of the hypothalamic-pituitary-gonadal axis, which determines the onset of menarche [ 29]. On the other hand, investigation for GnRH receptor mutations revealed that genetic variation in GnRH1 and GnRHR is not likely to be a substantial modulator of pubertal timing in the general population [ 33].

Recently, a genome-wide association (GWA) study was conducted aiming to identify common variants associated with the timing of puberty [ 34]. For age at menarche only one single nucleotide polymorphism reached genome-wide statistical significance, rs314276 in intron 2 of LIN28B on chromosome 6. Each major allele was associated with 0.12 years earlier menarche. This allele was also associated in girls with earlier breast development, in boys with earlier voice breaking and a faster tempo of growth and shorter adult height in both sexes.

Ethnic/racial differences in the timing of puberty and menarche

Several studies performed, especially in the USA, have shown ethnic-racial differences in pubertal maturation and menarche. Black girls were younger than white girls at the same stage of breast development, pubic hair development and menarche.

The Bogalusa Heart Study included data from 7 cross-sectional examinations of school-aged children, which were used for both cross-sectional and longitudinal analyses [ 35]. According to the study, black girls experienced menarche, on average, 3 months earlier than did white girls (12.3 vs 12.6 years) and during a 20 year study period, the median menarcheal age decreased by approximately 9.5 months among black girls. Secular trend among white girls was smaller and less consistent, since a 2 month decrease was recorded.

Anthropometric dimension differences between black and white girls, such as weight, height, and skinfold thickness, could be a confounding factor; however, controlling for height and either BMI or weight, the rate of early menarche remained significantly higher among black girls, suggesting that race is an independent factor of pubertal/menarcheal timing. The racial difference in pubertal maturation may reflect genetic factors. Black girls present higher insulin response to a glucose challenge, and subsequently increased levels of free IGF1, which is associated with skeletal and sexual maturation compared to white girls [ 36].

Moreover, another US study performed using data from the Third National Health and Nutrition Examination Survey, demonstrated that the mean age at onset of pubic hair, breast development and menarche was 9.5, 9.5, and 12.1 years for black girls; 10.3, 9.8, and 12.2 for Mexican American girls; and 10.5, 10.3 and 12.7 for white girls. The racial/ethnic differences remained even after adjustment for current body mass index and several social and economic variables [ 37].

Girls in South Europe experience menarche earlier than girls in North Europe. Mean menarcheal age in France and other Mediterranean countries is lower than in other Western European countries [ 38], which points to a geographical difference that reflects both genetic or ethnic and environmental factors. Geographical differences might involve altitude, temperature, humidity and lighting. Of special interest is that lighting signals on hypothalamus- pituitary- gonadal axis are supposed to be mediated through melanotonin circuit. According to several studies, menarche is more frequent in winter than in summer, which points to an inhibitory effect of photostimulation.

Age at menarche in Asian is similar to Mediterranean girls; mean menarcheal age in Hong Kong [ 39] and Japan [ 40] is 12.38 and 12.2 years, respectively, and in Greece [ 41] or Spain [ 42] 12.27 and 12.34, respectively.

Menarcheal age related to body fat, nutrition and physical activity

Body size parameters, such as weight or BMI and height are strongly correlated with the age at menarche. Frisch and Revelle proposed a critical body weight and weight gain for the onset of menarche [ 43, 44]. Higher subcutaneous fat levels and BMI at prepubertal ages (5-9 years) are associated with increased likelihood of early (<11 years) menarche [ 35]. Age at menarche is negatively related to hip and thigh circumference and positively related to waist circumference, status and biiliac breadth [ 45]. Blood leptin levels were also much more strongly related to gluteofemoral than upper body fat, suggesting that leptin may convey information about fat distribution to the hypothalamus during puberty [ 45]. The association of birth weight with pubertal development has not been yet well documented [ 46, 47], although there are data that in small for gestational age girls the age at both pubertal onset and menarche are advanced by about 5-10 months, whereas in boys pubertal onset usually occurs at an appropriate age [ 48]. On the other hand, Ellison related menarcheal age to height rather than weight, suggesting that skeletal maturation is more important than body fat accumulation for menarche [ 49], a finding that was also supported by a survey performed among schoolgirls in Taiwan [ 50].

Other studies have shown that rapid early infancy weight gain from birth to age 2 months, and also from 2 to 9 months, predicted subsequent greater adiposity, assessed by DXA at age 10 yr, and earlier age at menarche in girls. This association was not existent when weight gain occurred later in infancy, i.e. between 9 and 19 months of age [ 51].

Regarding nutritional habits, increased energy-adjusted intake was associated with early menarche [ 52]. The quality of food intake also influences puberty. Berkey et al [ 53] demonstrated that high animal versus vegetable protein ratio at the ages of 3-5 years is associated with early menarche, after controlling for BMI.

A cross sectional study performed in a group of Colombian university women demonstrated that age at menarche was positively associated with the practice of at least two hours daily of physical activity [ 54]. Menarche, on average, occurs later in athletes, including ballet dancers, than in the general population, with the exception of swimmers, suggesting that intense exercise delays puberty [ 55]. The most probable explanation for no delay in menarcheal age of swimmers is that the normal body fat composition of swimmers balances the negative hypothalamic effect on GnRH pulsatile exerted by intensive exercise.

Environmental influences on pubertal/menarcheal timing alteration

Socioeconomic factors or life setting, such as urban/rural residence, family size, family income, level of parental education, may also influence pubertal development. Girls from families with a high socioeconomic status experience menarche at an earlier age than girls from families with lower socioeconomic status [ 56]. Furthermore, higher parental education has been associated with earlier timing of puberty [ 56]. Absence of a biological father, the presence of half- and step-brothers is associated with early menarche, whereas the presence of sisters, especially older ones, in the household while growing up, was associated with delayed menarche [ 57]. The prevalence of early menarche is even higher when stepfather presence is combined with a stressful family environment and with maternal mood disorders [ 57]. Girls raised in urban environments have earlier menarcheal ages than those raised in rural environments [ 58].

Third World girls adopted in Western European countries present the pattern of early menarche, which indicates the role of transition from an underprivileged to a privileged environment as determinant of menarche [ 59]. It has been suggested that the premature sexual maturation may be triggered by the catch-up growth that these children present [ 60]. Other stresses like acute/chronic illnesses [ 61] or war conditions [ 62] suppress the hypothalamic- pituitary-gonadal axis and delay pubertal onset.

Various studies focus on the role of environmental chemicals, called endocrine-disruptor chemicals (EDC), on puberty timing alteration. EDC are used as industrial solvents/lubricants [polychlorinated biphenyls (PCBs), polybrominated biphenyls (PBBs), dioxins], plastics [bisphenol A (BPA)], plasticizers (phthalates), pesticides [methoxychlor, chlorpyrifos, dichlorodiphenyltrichloroethane (DDT)], fungicides (vinclozolin), and pharmaceutical agents [diethylstilbestrol (DES)] [ 63]. Endocrine disruptors may have structural similarity with estrogen, thus their action is performed through estrogen receptor, whereas others, e.g. vinclozolin, interact with the androgen receptor, while other EDC, e.g. fadrozole and ketoconazole, inhibit aromatase or steroidogenesis, respectively. Furthermore, EDC may affect puberty via CNS regulation. For example, atrazine delays puberty in both males and females, reducing circulating LH and prolactin [ 64]. Phthalates and polychlorinated biphenyls have been associated with earlier breast development and menarche, respectively [ 65]. EDC may also influence the endocrine system in a harmful manner, inducing human disorders of sex differentiation [ 66] and hormone- dependent cancers [ 67].

Health implications of early or late menarche

Early puberty is associated with increased body mass index, insulin resistance, total number of metabolic syndrome components and hence increased cardiovascular risk [ 68]. Moreover girls with early menarche exhibit elevated blood pressure and glucose intolerance compared with later maturing girls, independent of body composition [ 69]. A recent large population-based Caucasian cohort study also confirmed these observations, but also correlated in a non-linear significant manner the earlier age at menarche (<12 yrs) with higher incident cardiovascular disease, incident coronary heart disease, all-cause mortality and cancer mortality after adjustment for age, physical activity, smoking, alcohol, educational level, occupational social class, oral contraceptive use, hormone replacement therapy, parity, BMI and waist circumference. Most of the subjects had a positive family history of heart attack, which indicates that this association may be partly mediated by increased adiposity but genetic mechanisms may contribute as well [ 70].

It has also been reported that menarcheal age influences bone mineral density and consequently the incidence of lumbar spine and hip fractures. Girls menstruating earlier have slightly higher bone mineral density of the lumbar spine and femoral neck in older age after excluding subjects who took hormone replacement therapy and adjusting for BMI [ 71]. This might be apparently explained due to longer lifetime exposure to the protective effects of endogenous estrogens at the period of acquisition of peak bone mineral density. On the other hand, late menarche is associated with osteoporosis, since studies including postmenopausal women suggest that those having later menstruated have lower mineral density at forearm, spine and proximal femur and increased risk of fractures as well [ 72, 73]. Moreover, apart from older women, onset of menstruation is a determinant factor of peak bone mineral density in young women. According to a Japanese cohort study, late menarche (>14 yrs) is associated with approximately 2- fold increased risk of low areal bone mineral density at the hip in women aged under 40 years [ 74]. Age at menarche correlates not only with bone mineral density but also with bone microstructure, since young healthy women with late menarche display lower total volumetric bone mineral density, cortical volumetric bone mineral density, and cortical thickness at forearm, a finding compatible with less endocortical accrual [ 75]. Finally, recent data suggest that in girls experiencing menarche later, the deficit of areal bone mineral density is generated before the onset of pubertal maturation with very mild increment during the whole period of pubertal maturation. This observation indicates that estrogen exposure is not the only key factor responsible for the influence of menarcheal age on peak bone mineral density and that other genetic determinants could be involved [ 76].

Multiple studies confirm that early menarche is a risk marker for breast cancer [ 77]. This predisposition is enhanced by the observation that earlier onset of menarche is accompanied by abdominal- type obesity and thus higher circulating levels of insulin, testosterone and insulin- like growth factor 1, which in turn act as growth factors for mammary tissue proliferation and are likely to promote mammary gland carcinogenesis [ 78].

Early menarche leads to earlier sexual intercourses and is a risk factor for adolescent depression [ 79]. Girls associate a variety of negative physical and psychological changes with menstruation, reflecting both misconception and ignorance [ 80] and the fear of being different from peers as well [ 81]. Girls' attitudes and expectations about menstruation are negatively biased and have been found to contribute to self- objectification, body shame, and lack of agency in sexual decision making [ 82]. Early maturing adolescents with problematic peer relations experience elevated social anxiety symptoms [ 83]. A recent research combined accelerated sexual maturation with negative experiences with the opposite sex, indicating that the earlier the menarche, the larger the estimated egocentric distance of virtual male voices and the more negative the evaluations of male faces [ 84]. Moreover, if early maturation is combined with social factors, such as an underprivileged neighbourhood, susceptibility to a violent behaviour enhances [ 85]. On the other hand, girls with constitutional delay in puberty and onset of menstruation feel that this delay has an impact on school, work or social status and would prefer to accelerate their growth spurt by treatment [ 86].

A summary of the health implications of early or late menarche are shown on Table .

Table 2

Abdominal type obesity

Osteoporosis

Insulin resistance

Adolescent depression

Glucose intolerance

Social anxiety symptoms

Cardiovascular risk

Coronary heart disease

Increased bone mineral density

Increased cancer mortality

Conclusions

The improvement of socioeconomic conditions that took place in the 20 th century resulted in an earlier onset of puberty in children, indicated by the fall of the age at menarche. However, there are reports from industrialized countries that this trend has been leveling off.

Onset of puberty is controlled by a complex neuronal network, Kiss1 gene, that produces Kisspeptin, and its receptor, G Protein Coupled Receptor 54 (GPR54) having a key role in pubertal onset and reproduction. Recently, a single nucleotide polymorphism of LIN28B on chromosome 6 was associated with earlier menarche.

Besides genetics, menarche is also influenced by socioeconomic and environmental factors. Race, BMI, geography, nutritional habits, exercise all have been shown to influence menarcheal age; furthermore, Third World girls adopted in developed countries present early menarche. Moreover, endocrine-disruptor chemicals result on puberty timing alteration.

Menarcheal age has important health implications, as early menarche is associated with more cardiovascular incidents and higher all cause, including cancer, especially of the breast, mortality. Late menarche is associated with osteoporosis and increased fracture risk. Moreover, early menarche has been related to anxiety symptoms, depression, premature intercourse and violent behavior.

More studies are needed in order to predict which girls may develop metabolic or psychological disturbances due to early menarche and whether they can be benefited by medical manipulation of the pubertal events.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

AP conceived of the report, helped to draft the manuscript and in figure and tables' design. OK carried out literature research and drafted the manuscript and the tables as well. Both authors read and approved the final manuscript.

References

Heidi DH. Yearbook of Phys Anthropol. 1. Vol. 29. 1986. Menarcheal age in Europe; pp. 81-112. [[CrossRef] Google Scholar]

Tanner JM. Foetus into Man. 2. Ware: Castlemead Publications; 1989. [Google Scholar]

Cameron N. In: Human Growth and Development. Cameron N, editor. Academic Press, San Diego, Ca; 2002. Assessment of maturation; pp. 363-382. full_text. [Google Scholar]

# data[].attributes.attachment_link.description
Menarche is a milestone in a woman's life as it denotes the start of reproductive capacity. Aim of this report is to review the recent developments and the current knowledge in the neuroendocrinology of pubertal onset and the factors, genetic and environmental, ...

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Delayed Puberty in Girls With Cystic Fibrosis Despite Good Clinical Status

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Abstract

Background.  Previous studies have shown that puberty is delayed among patients with cystic fibrosis (CF). Malnutrition has been considered the main etiologic factor. Today with improved medical therapy and nutritional support, most CF patients obtain an almost normal nutritional status.

Objectives.  To investigate whether pubertal development among female CF patients at the Stockholm CF Center was normal and, if not, what other parameters besides nutrition might influence this.

Methods.  Seventeen patients were studied retrospectively regarding age at peak height velocity and menarche. Menarcheal age (MA) was compared with normal population data and related to clinical and nutritional status, genotype, oral glucose tolerance test (OGTT), and essential fatty acid levels.

Results.  The mean age at peak height velocity (12.9 ± 0.8 years) and at menarche (14.9 ± 1.4 years) was significantly higher in the CF patients compared with normal controls (11.9 ± 1.0 years and 13.0 ± 1.0 years, respectively). No correlation was found between menarchal age and nutritional or clinical parameters. The patients with pathological OGTT without overt diabetes were significantly older at menarche (15.8 ± 1.7 years) compared with the patients with normal OGTT (14.3 ± 0.9 years). The patients who were homozygous for the most common mutation, deltaF508, were significantly older at menarche (15.2 ± 1.9 years) than those who were not (14.7 ± 0.9 years).

Conclusions.  Pubertal delay still existed among the CF patients despite good clinical status. The patients homozygous for deltaF508 and those with pathological OGTT showed the most delayed puberty.

# data[].attributes.attachment_link.title
Delayed Puberty in Girls With Cystic Fibrosis Despite Good Clinical Status

# data[].attributes.attachment_link.description
Background.  Previous studies have shown that puberty is delayed among patients with cystic fibrosis (CF). Malnutrition has been considered the main etiologic factor. Today with improved medical therapy and nutritional support, most CF patients obtain an almost normal nutritional status. Objectives.

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Associations of urinary phthalate and phenol biomarkers with menarche in a multiethnic cohort of young girls.

Wolff et al. 2017. Reproductive Toxicology Vol. 67: 56-64.

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Role of Environmental Factors in the timing of Puberty
Susan Y. Euling, PhD,
doi:10.1542/peds.2007-1813C

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The Neuroendocrine Timing of Puberty: Francis JP Ebling. 2005. Reproduction. Vol 129(6): 675-683

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Psychological effects of gonadotropin-releasing hormone agonist treatment in girls with central precocious puberty

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The Timing of Puberty: Is it changing? Does it Matter?

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Adverse Childhood Experiences and Early Pubertal Timing Among Girls: A Meta-Analysis

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Adverse Childhood Experiences and Early Pubertal Timing Among Girls: A Meta-Analysis

Department of Maternal, Child & Adolescent Health, School of Public Health, Anhui Medical University, 81th Meishan Road, Hefei 230032, Anhui Province, China

Author to whom correspondence should be addressed.

Received: 24 July 2019 / Accepted: 10 August 2019 / Published: 13 August 2019

abuse; pubertal timing; adversity; adverse childhood experiences; meta-analysis

1. Introduction

The onset of puberty is pivotal for human growth and development [ 1]. However, among developed nations, there has been a secular trend of early pubertal timing over the past century, and in recent years, also in developing countries [ 2, 3]. Early pubertal timing has been recognized as a risk factor for adverse health outcomes in adulthood including obesity, hyperinsulinemia, type-2 diabetes, hypertension, coronary heart disease, depression and early mortality [ 4, 5, 6, 7, 8]. Multiple inter-related social and environmental factors have been found to significantly influence pubertal timing, including nutrition and obesity, genetic factors, and general health status, race, and familial socioeconomic status (SES) [ 9].

Adverse childhood experiences (ACEs), defined as experiences that threaten the child's bodily, familial, or social safety or security, classically include maltreatment and household dysfunction to more targeted experiences of bullying, exposure to crime, victimization, and economic disadvantage [ 10]. For the purposes of this meta-analysis, ACEs were defined as exposure to at least one significant form of the following childhood adversities: before the age of 18 years: physical abuse, sexual abuse, neglect (failure to provide and failure to supervise physically or emotionally), family dysfunction (parental death or serious illness, parental separation or divorce, parental incarceration, parental substance abuse, domestic violence, mental illness), low SES, and father absence (separation or divorce of the birth parents followed by absence of the birth father from the home).

ACEs are a major public health problem, with some estimates suggesting that about a third of the general population may be affected [ 11]. A growing number of studies have examined ACEs as risk factors for early pubertal timing, however, the association has been a topic of enduring controversy [ 3, 9, 12, 13, 14, 15, 16]. For example, Romans et al. [ 16] have found associations between father absence and early puberty whereas similar results were not observed by Henrichs et al. [ 9].

The life history theory provides a theoretical framework for explaining the individual differences in reproductive strategies from adolescence to adulthood, especially the role of family and ecological environment in regulating individual differences in puberty development and reproductive strategies. It attempts to explain the timing of reproductive development and events across the life span in terms of evolved strategies for distributing metabolic resources between the competing demands of growth, maintenance, and reproduction [ 17]. Specifically, there are environmental conditions in which accelerated maturational development is an adaptive response serving to maximize reproduction opportunities. Based on the life history theory, three middle-level life history models have been advanced to explain why ACEs may increase risk of early pubertal timing. First, the psychosocial acceleration theory, first advanced by Belsky, Steinberg, and Draper, 1991 postulates that ecological stressors in and around the family create conditions that undermine parental functioning and lower the quality of parental investment [ 18]. Under these conditions, parental investment is unreliable and/or not closely related to the reproductive success of offspring, girls are predicted to develop in a manner that accelerates pubertal maturation and sexual activity, and orients the individual towards unstable pair-bonds. Second, as a variant of the psychosocial acceleration theory, paternal investment theory parallels this logic but posits a more unique and central role for father and other men in the regulation of female pubertal timing, separate from the effects of other dimensions of psychosocial stress and support in the child's environment [ 17]. The third theory is an extension on the psychosocial acceleration theory and paternal investment theory and is referred to as the child development theory. The child development theory describes how the composition and quality of family environments might influence the length of childhood as a developmental strategy. According to child development theory, the benefits of a longer childhood (delay puberty) are increased in high-quality family contexts that foster the development of sociocompetitive competencies, while the costs of cutting short childhood (accelerate puberty) are reduced in adverse family contexts that do not significantly facilitate these competencies. Children should be selected to take advantage of the benefits of high-quality parental investment and reduce the costs of low-quality parental investment by contingently altering the length of growth and development prior to reproductive maturity [ 17, 19].

Activation of the hypothalamic-pituitary-adrenal (HPA) axis may be an underlying neuroendocrine mechanism linking ACEs and early pubertal timing, which governs both stress response and adrenarche, the first phase of pubertal maturation [ 20]. ACEs can alter the response of the HPA axis, with chronic stressful experiences resulting in hyperactivation followed by downregulation of the stress system. The attenuated cortisol profile may actually hasten the pubertal timing because the stress function of the HPA axis is dampened, allowing the cascade of pubertal hormones via the HPG axis to commence [ 21]. However, given the different forms of ACEs and the multiple indicators of HPA axis, more longitudinal studies are needed to understand the underlying mechanism better.

Variability in study design, methodology, subject characteristics, type of ACEs, and developmental timing limit the ability to draw definitive conclusions. The objective of this meta-analysis was to clarify the relationship between ACEs and early pubertal timing by means of a systematic examination of the literature, which may be beneficial for guiding future empirical and theoretical work in this area.

2. Materials and Methods

2.1. Search Strategy

The study was performed according to the recommendation of the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) guidelines [ 22]. A systematic database search from 1980 up to 2018 was performed on PubMed and Web of Science using the following search themes: ("ACE", "ACEs", "adverse childhood experiences", "adverse childhood events", "childhood maltreatment", "child maltreatment", "childhood adversity", "child adversity", "childhood adversities", "child adversities", "early adversity", "early adversities", "childhood physical abuse", "child physical abuse", "physical abuse", "childhood sexual abuse", "child sexual abuse", "sexual abuse", "childhood neglect", "child neglect", "childhood physical neglect", "child physical neglect", "physical neglect", "child abuse", "childhood abuse"; "child emotional abuse", "childhood emotional abuse", "emotional abuse", "child emotional neglect", "childhood emotional neglect", "child trauma", "childhood trauma", "emotional neglect", "parental incapacities", "family incapacities", "adverse family experiences", "adverse family events", "trauma", "poverty"; "socioeconomic status", "parental loss", "adversity", "early life stress", "bullying") combined with pubertal timing related search terms ("puberty", "pubertal status", "early puberty", "early pubertal timing", "age of menarche", "early age of menarche", "early maturation", "pubertal timing"). In addition, we searched the bibliographies of the articles found on the subject [ 14, 23]. The present analysis focused on childhood sexual abuse, physical abuse, neglect, father absence, low SES, family dysfunction. All the included studies were published in English and from peer-reviewed journals.

2.2. Inclusion Criteria and Exclusion Criteria

Selection criteria for the meta-analysis included articles exploring the association between ACEs and early pubertal timing. We excluded review articles, editorials, commentaries, and animal studies. The life history theory to pubertal timing pivots around the trade-off between the allocation of resources to physical growth versus production of offspring, which is particularly relevant to females. It has been applied more broadly and successfully to the question of female rather than male pubertal timing. In addition, there is a clear and easily assessed marker of female but not male pubertal timing: age at menarche [ 17]. Given the theoretical and empirical reasons, we included female participants only.

The majority of studies utilized age at menarche, Tanner staging scores, Pubertal Development Scale (PDS) and relative perceived timing questions to the evaluation of pubertal developmental. For studies using age at menarche, menarche occurring before the age of 11 years was considered as early pubertal timing, while after the age of 14 years as delayed pubertal timing. For those studies only reporting the correlation between ACEs with age at menarche, negative direction suggested that ACEs was associated with early pubertal timing. For studies using Tanner staging and the PDS, pubertal timing was then examined such that early pubertal timing were adolescents who scored two standard deviations above the mean and late pubertal timing were two standard deviations below the mean. Some studies also trichotomized pubertal timing groups, such that one standard deviation above the mean was categorized as early. Some studies used a single self-report item to assess relative perceived timing of puberty. Generally, this item was stated as follows "Compared with other boys/girls your age, would you say your physical development has developed 'much earlier,' 'somewhat earlier,' 'about the same,' 'somewhat later,' or 'much later' than other boys or girls your age?" Due to the considerable variation in the measurement method of pubertal timing, subgroup analysis was performed to examine significant sources of this heterogeneity [ 24].

2.3. Risk of Bias Assessment

Two reviewers independently assessed the methodology quality of included cohort studies using the Newcastle-Ottawa Scale (NOS) (range, 0 to 9 scores) [ 25]. Assessment items included the selection (four items, four scores), comparability (one item, two scores), and assessment of outcome (three items, three scores). Studies are then stratified by score: low quality (scored 0-3), medium quality (scored 4-6), and high quality (scored 7-9). The cross-sectional study quality was assessed using the Agency for Healthcare Research and Quality guidelines [ 26]. Studies are then stratified by score: low quality (scored 0-3), medium quality (scored 4-7), and high quality (scored 8-11). The third reviewer was involved when any disagreements existed. The quality scores did not affect studies for inclusion but were considered when performing sensitivity analysis and interpreting our research results.

2.4. Data Screening and Extraction

After duplicate citations were removed, two reviewers independently screened the titles and abstracts to identify potentially relevant citations. Then the potentially eligible studies were then screened again by full texts. The pre-designed criteria mentioned above were used to guide the entire process of screening. Subsequently, the following data were extracted from all the included studies using a pre-designed extraction form by two reviewers: (1) general information, including authors, publication year, (2) study design and specific types of ACE, (3) sample size, (4) the measure of ACEs, (5) the measure of early pubertal timing. The third reviewer was involved when any disagreements existed.

2.5. Effect Size Computation and Statistical Analyses

All analyses were carried out using the meta-analysis commands of Stata 11.0. For each study, we computed an effect size Cohen's d [ 27] using the effect size calculator [ 28] for the association between ACEs and early pubertal timing. Cohen's guidelines [ 27] were used to interpret effect sizes such that effects sizes of ds = 0.20 were considered small, ds = 0.50 were considered moderate, and ds = 0.80 were considered large. If correlations (r) or odds ratios (OR) were reported, they were converted to Cohen's d using the formulas d = 2r/(1 − r ²) 1/2 [ 29] or d = 3 1/2/πlog (OR) [ 30], respectively. To examine the global association between ACEs and early pubertal timing, a meta-analysis was carried out on the effects extracted from studies providing a summary measure of exposure to ACEs [ 31]. Unadjusted values were calculated in the program, thus avoiding biases that may have arisen from adjustments to different confounders done in each study. Heterogeneity was calculated using the Q test and I ² statistic and the values of I ² metric 25%, 50%, and 75% were considered as low, medium, and high heterogeneity [ 32]. The effect of specific types of ACEs (i.e., sexual abuse, physical abuse, neglect, father absence, low SES, family dysfunction) were tested in this meta-analysis. Due to the large overlap, these analyses were treated as independent research syntheses and no attempt was made to statistically compare these effects using meta-regression or subgroup analyses. We did sensitivity analyses by excluding outlying studies. We explored risk of publication bias using the Egger tests when sufficient studies were included in the meta-analysis (at least 10 samples).

Planned meta-regressions and subgroup analyses were conducted to explore possible sources of heterogeneity. We did univariate analyses to test the individual association of the covariates (sample size, publication year) with pooled estimates. Subgroups were delineated using the following criteria: ACEs measure (questionnaire, interview, and combination), pubertal timing measure (age at menarche, number of early menarches, PDS, Tanner stage), original variable type (categorical, continuous and others), as well as study design (cross-sectional and longitudinal).

3. Results

3.1. Search Results

As illustrated in Figure 1, after duplicates removed, the search strategy resulted in 3002 records, of which 2767 were excluded following title and abstract, and a further 193 were excluded following review of the full text, 42 studies with 45 independent data sets met full inclusion criteria. Table 1 summarizes the characteristics of the eligible studies. 26 articles used data from cross-sectional studies and 16 used data from longitudinal studies.

3.2. Association between Total ACEs and Early Pubertal Timing

Figure 2 shows the association between total ACEs (n = 35) and early pubertal timing, with an effect of Cohen's d: −0.04 (95% CI: −0.14, 0.06). The Q and I ² tests indicated that the association between total ACEs and early pubertal timing was statistically heterogeneous (I ² = 99%, p < 0.001), subgroup analyses were performed to examine significant sources of this heterogeneity. Egger's test (B = 2.21, SE = 2.17, p = 0.32) showed no evidence of substantial publication bias. We examined possible changes in the effects by omitting one study at a time in the analysis but did not find any meaningful changes. Analyzing all studies except Tahirović HF et al. [ 61] on account of its indefinite type of ACEs, we obtained a significant results with an effect of Cohen's d: −0.09 (95% CI: −0.17, −0.01), but the heterogeneity was still considerable (I ² = 98.3%, p < 0.001). We excluded Alvergne et al. [ 36], which had a huge outlier value, from the analysis. Using the random effect model, we got a pooled Cohen's d: 0.04 (95% CI: −0.05, 0.14), suggesting that the association between total ACEs and delay puberty was still small and not significant.

3.3. Associations between Specific Types of ACEs and Early Pubertal Timing

The pooled effect size of specific types of ACEs are presented in Table 2. Influence analyses were performed on each type of adversities, we did not find any meaningful changes. We found that the effect for sexual abuse (Cohen's d −0.14 (95% CI −0.18, −0.11), I ² = 72.4, p < 0.001) and family dysfunction (Cohen's d −0.08 (95% CI −0.11, −0.04), I ² = 66.9, p = 0.001) was small, while father absence (Cohen's d −0.40 (95% CI −0.63, −0.16), I ² = 98.2, p < 0.001) was between small to medium. When we excluded Alvergne et al. [ 36], the effect size of father absence was reduced by nearly half (Cohen's d −0.19 (95% CI −0.27, −0.11), I ² = 83.2, p < 0.001). We did not observe significant associations in other types of ACEs, or across total ACEs.

Except for physical abuse, neglect and low SES, the association between ACEs and early pubertal timing was small but significant, and the pooled effect size was highest for father absence and the least for family dysfunction. We found considerable heterogeneity between estimates for almost all of the outcomes. Heterogeneity between estimates was higher for father absence and lower for sexual abuse, relatively. Meta-regression revealed that the publication years (p = 0.083) and sample size (p = 0.661) in the primary studies did not influence the observed effect sizes.

Subgroup analyses are presented in Table 3. After subgroup analysis by ACEs measure (questionnaire, interview and combination), pubertal timing measure (age at menarche, number of early menarche, PDS, Tanner stage), original variable type (categorical, continuous and others), as well as study design (cross-sectional and longitudinal), heterogeneity between estimates is still considerable. In the subgroup analysis by pubertal timing measure, the pooled effect size was small but significant in studies measuring pubertal timing by a number of early menarche and Tanner stage. Pooled effect size of one study measuring pubertal timing by Tanner stage was Cohen's d: −0.27 (95% CI: −0.52, −0.03) [ 12]. Similarly, in subgroup analysis by original variable type, the pooled effect size for categorical was small but significant.

4. Discussion

To our knowledge, this is the first meta-analysis to examine the association between ACEs and early pubertal timing and has extended previous studies by quantifying the effect size for early pubertal timing. Our finding suggests that sexual abuse, father absence, and growing up with challenging family circumstances were significantly associated with early pubertal timing among girls. Using Cohen's categorization, the effect for sexual abuse and family dysfunction is small, while father absence is between small to medium. However, similar associations were not observed in other types of ACEs, or across total ACEs.

Herman-Giddens et al. [ 67] first reported in 1997 that child sexual abuse increased the risk of girls' pubic hair and breast development before age 8. Subsequent studies have consistently found that sexual abuse was associated with early pubertal timing [ 16, 42, 43]. Recently, a cohort study of the Avon Longitudinal Study of Parents and Children (ALSPAC) mothers showing that total ACEs was not associated with age at menarche, while childhood sexual abuse was associated with lower age at menarche, which is consistent with our findings [ 54]. Sexual abuse is often regarded as the most prevalent health problem children face with the most serious array of consequences, while in our study, early pubertal timing may be more affected by father absence instead of sexual abuse.

As early as the 1980s to the 1990s, Draper and Harpending [ 68] and Belsky et al. [ 18] began to focus on the association between father absence and reproductive behaviors in adulthood, which has received increased attention over recent years. Majority of these studies have indicated a significant association between father absence and early pubertal timing. A study from a large UK birth cohort (ALSPAC) demonstrated that girls from father-absent homes had earlier menarche than girls from father-present homes [ 46]. The observed association between father absence and early pubertal timing has also been supported by other articles [ 20, 23]. Moreover, the earlier that father absence occurs, the earlier girls tend to experience puberty, there is evidence to suggest that exposure to father absence during the first five years of life is more strongly associated with early menarche than father absence later in childhood [ 24].

It has been previously argued that the effects of age at menarche may be explained by low SES arising as a result of father absence, for example, decrease in family income, major financial problems [ 69]. However, in this meta-analysis, we did not find a significant association between low SES and early pubertal timing. When we excluded studies in which pubertal timing measured by Tanner stage or PDS [ 12, 15, 23, 60], results suggested that girls living in low SES households may experience delayed onset of menarche (Cohen's d: 0.12, 95% CI: 0.003, 0.25). A longitudinal study on 1091 black and 986 white girls from the three sites in the United States found that high SES was a protective factor for the risk of early menarche among white girls but opposite among black girls [ 14]. Given the challenges in methodology and definition of SES along with socially heterogeneous of study populations, it is difficult to draw firm conclusions concerning the relationship between low SES and early pubertal timing.

The association between family dysfunction and early pubertal timing was weak, we suspect that family dysfunction may be a proxy variable that represents a range of other family characteristics (including parental divorce, separation, mental illness, and family conflict) and have an effect similar to father absence. However, when we excluded three articles involving parental divorce or separation, the effect size was small but still significant. The effect of total ACEs on adolescent development was not significant. One explanation may be that there are great individual differences in the types, timing, duration, and severity of ACEs. Another explanation is that the association may differ depending on race/ethnicity. As demonstrated in prior research, high SES was a protective factor for the risk of early menarche among white girls but opposite among black girls [ 14].

Overall, despite some inconsistencies across specific forms of ACEs with early pubertal timing, these results support that ACEs exposure may affect female reproductive function. Given the association between ACEs and early pubertal timing, clinicians should sensitively enquire about past childhood experiences, and tailor support accordingly, thus resetting their trajectory for lifelong health and reducing the risk of chronic diseases and conditions.

There are also several limitations. Firstly, most of the measurements relied on retrospective self-report which is subject to recall or reporting biases. Secondly, this sample was restricted to females, and these findings cannot be extrapolated to males. In addition, the analysis revealed substantial statistical heterogeneity, which allows for less confidence in the estimated effect sizes, but is not surprising given the methodological and analytic variances in the identified studies. We cannot rule out the effect of interactions of ACEs with other factors (parental early puberty history, physical activity, etc.) in the current meta-analysis because most studies did not adjust for these interactions, or partly adjusted for these factors as possible moderators. The current meta-analysis focused on specific types of ACEs (sexual abuse, physical abuse, neglect, father absence, low SES, and family dysfunction). Nevertheless, adversity is a heterogeneous concept (including types of ACEs not considered here, such as bullying, exposure to war, and natural disasters, etc.). Although most studies measured ACEs at any point in childhood or adolescence, we were unable to obtain sufficient information about the frequency, timing, and duration of ACEs. Additionally, studies without sufficient statistical information for the computation of effects were not included in our analysis. Nevertheless, the thorough search of literature ensures a full coverage of the existing evidence and makes the results more convincing. Moreover, the large sample of the study population derived from the included studies enhances the possibility of effect detection with reasonable statistical power.

These limitations also suggest some directions for future research. Identification of distinct dimensions, duration and sensitive periods of adverse childhood experience that differentially influence pubertal development are required to uncover mechanisms that explain how childhood adversity is associated with female reproductive strategies.

5. Conclusions

In summary, our analyses indicate that father absence is more strongly related to early pubertal timing among girls, followed by sexual abuse and family dysfunction. Additional research is needed to better understand the mechanisms driving these relationships. Due to the high heterogeneity, a conclusive statement on the effect size of the association between ACEs and early pubertal timing should be made with caution.

Author Contributions

Y.S. and L.Z. contributed to the conception and design of the review. L.Z. applied the search strategy. L.Z. and D.Z. applied the selection criteria. L.Z. and D.Z. completed the assessment of risk of bias. L.Z. and Y.S. analyzed the data and interpreted data. L.Z. and Y.S. drafted this manuscript. All authors edited this manuscript.

Funding

This work was supported by the National Natural Science Foundation of China [grant number 81872638] and Natural Science Foundation for Distinguished Young Scholars of Anhui Province [grant number 1908085J26].

Conflicts of Interest

The authors declare no conflicts of interest.

References

1. Agency for Healthcare Research and Quality. Methods Guide for Effectiveness and Comparative Effectiveness Reviews. Available online: http://effectivehealthcare.ahrq.gov/index.cfm/search-for-guides-reviews-and-reports/?pageaction = displayproduct&productid = 318 (accessed on 13 July 2018).

2. Cohen, J. Statistical Power Analysis for the Behavioral Sciences, 2nd ed.; Lawrence Erlbaum Associates: New York, NY, USA, 1998. [Google Scholar]

3. Effect Size Calculator. Available online: https://cebcp.org/practical-meta-analysis-effect-size-calculator/standardized-mean-difference-d/means-and-standard-deviations/ (accessed on 13 July 2018).

4. Bornstein, M.; Hedges, L.V.; Higgins, J.P.T.; Rothstein, H.R. Introduction to Meta-Analysis; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2009. [Google Scholar]

5. Tekgül, N.; Saltık, D.; Vatansever, K. Secular trend of menarche age in an immigrant urban city in Turkey: Izmir. Turk. J. Pediatr. 2014, 56, 138-143. [Google Scholar]

# data[].attributes.attachment_link.title
Adverse Childhood Experiences and Early Pubertal Timing Among Girls: A Meta-Analysis

# data[].attributes.attachment_link.description
The association between adverse childhood experiences (ACEs) and pubertal timing has been a topic of enduring controversy. A systematic search of PubMed and Web of Science databases was undertaken to quantify the magnitude of total and specific forms of ACEs effects on early pubertal timing among girls.

# data[].attributes.body
Endocrine Disrupters and Possible Contribution to Pubertal Changes
Julie Fudvoye, et al.
Doi:https://doi.org/10.1016/j.beem.2019.101300

# data[].attributes.body
Endocrine Disrupters and Pubertal Timing

Louise C. Greenspan, M.D and  Mary M. Lee, M.D., FAAP

doi: 10.1097/MED.0000000000000377

# data[].attributes.attachment_link.title
Endocrine Disrupters and Pubertal Timing

# data[].attributes.body
Metabolic control of puberty: Roles of leptin and kisspeptins

Author links open overlay panel by Miguel A.Sanchez-GarridoManuelTena-Sempere

https://doi.org/10.1016/j.yhbeh.2013.01.014

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Detailed Record

Title:

Author:

Ye, Xiaoqing; Jing Liu; Shilin Zhao; Weiping Liu; Wuye Pan; Yimin Zhu; Yuehao Zhao

Source:

Environmental pollution, 2017, , p. .

Publisher:

Elsevier Ltd

Abstract:

Pyrethroids, a class of ubiquitous insecticides, have been considered as endocrine-disrupting chemicals (EDCs). Female animal studies suggested that early-life pyrethroids exposure might delay puberty onset. However, it remains unclear whether this association applies to human populations. A total of 305 girls at the ages of 9©Ø℗€℗"15 years old were recruited in Hangzhou, China in this study. The concentration of the common metabolite of pyrethroids, 3-phenoxybenzoic acid (3-PBA), was analyzed in urine samples to reflect the exposure level of pyrethroids. The associations of 3-PBA with pubertal stages were evaluated using a multinomial logistic regression model. The geometric mean level of 3-PBA was 1.11©‚℗ ©Ž℗ơg/L (1.42©‚℗ ©Ž℗ơg/g for creatinine-adjusted concentration). There was a significant 45% reduction in odds of being in breast stage 3 (B3) per one-unit increase in the log-transformed 3-PBA levels [OR©‚℗ =©‚℗ 0.55 (95%CI: 0.31©Ø℗€℗"0.98), p©‚℗ =©‚℗ 0.042]. A similar negative association was found between urinary 3-PBA levels with later onset by pubic hair stage 2 (P2) [OR©‚℗ =©‚℗ 0.56 (95%CI: 0.36©Ø℗€℗"0.90), p©‚℗ =©‚℗ 0.015]. Similar negative association was also observed between urinary 3-PBA levels and pubertal onset indicated by menarche [OR©‚℗ =©‚℗ 0.51 (95%CI: 0.28©Ø℗€℗"0.93), p©‚℗ =©‚℗ 0.029]. For the first time to our knowledge, this work reveals that pyrethroids exposure may increase the risk of delayed pubertal onset in girls.

Descriptors:

breasts; Chinese people; endocrine-disrupting chemicals; girls; human population; insecticides; menarche; metabolites; puberty; pyrethrins; regression analysis; risk; urine; China

Identifiers:

3-Phenoxybenzoic acid (3-PBA); Menarche; Puberty; Pyrethroids; Tanner stages

Genre:

article

Language:

English

Publication Type:

Journal Article

Note:

Pre-press version.

ISSN:

02697491

URL:

http://dx.doi.org/10.1016/j.envpol.2017.04.035

Subset:

Indexing Branch - NAL

Publication Date:

Jan 1, 2017

Update Code:

00000000

Accession Number:

IND605674103

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Association of pyrethroids exposure with onset of puberty in Chinese girls

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Title: Author: Ye, Xiaoqing; Jing Liu; Shilin Zhao; Weiping Liu; Wuye Pan; Yimin Zhu; Yuehao Zhao Source: Environmental pollution, 2017, , p. . Publisher: Elsevier Ltd Abstract: Pyrethroids, a class of ubiquitous insecticides, have been considered as endocrine-disrupting chemicals (EDCs). Female animal studies suggested that early-life pyrethroids exposure might delay puberty onset.

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Relationship of Age for Grade and Pubertal Stage to Early Initiation of Substance Use.
Suggested citation for this article: Dudovitz RN, Chung PJ, Elliott MN, Davies SL, Tortolero S, Baumler E, et al. Relationship of Age for Grade and Pubertal Stage to Early Initiation of Substance Use. Prev Chronic Dis  2015;12:150234. DOI: http://dx.doi.org/10.5888/pcd12.150234.

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Urinary bisphenol A and age at menarche among adolescent girls: Evidence from NHANES 2003–2010
Laura A. Mcguinn, Armen A. Ghazarian, L.Joseph Su, and Gary L. Ellison. 2015. Urinary bisphenol A and age at menarche among adolescent girls: Evidence from NHANES 2003–2010. Environmental Research 136 (2015), 381–386. doi:http://dx.doi.org/10.1016/j.envres.2014.10.037

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Puberty and depression: the roles of age, pubertal status and pubertal timing
A.Angold, E. J.Costello, and C. M.Worthman
ANGOLD, A., COSTELLO, E., & WORTHMAN, C. (1998). Puberty and depression: The roles of age, pubertal status and pubertal timing. Psychological Medicine, 28(1), 51-61. doi:10.1017/S003329179700593X

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Background. Previous work has indicated that the 2[ratio ]1 female[ratio ]male sex ratio in unipolar depressive disorders does not emerge until some time between ages 10 and 15.

Methods. Data from four annual waves of data collection from the Great Smoky Mountains Study (GSMS) involving children aged nine to 16 were employed.

Results. Pubertal status better predicted the emergence of the expected sex ratio than did age. Only after the transition to mid-puberty (Tanner Stage III and above) were girls more likely than boys to be depressed. The timing of this transition had no effect on depression rates. Before Tanner Stage III, boys had higher rates of depression than girls, and the prevalence of depression appeared to fall in boys at an earlier pubertal stage than that at which it began to rise in girls. In addition, recent transition to Tanner Stage III or higher had a transient effect in reducing the prevalence of depression in boys.

Conclusions. The period of emergence of increased risk for depression in adolescent girls appears to be a relatively sharply demarcated developmental transition occurring in mid-puberty. Previously reported effects of the timing of puberty (which have tended to be transient) appeared less important in increase of risk for depression than pubertal status.

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Puberty and depression: the roles of age, pubertal status and pubertal timing | Psychological Medicine | Cambridge Core

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Background. Previous work has indicated that the 2[ratio ]1 female[ratio ]male sex ratio in unipolar depressive disorders does not emerge until some time between ages 10 and 15. Methods. Data from four annual waves of data collection from the Great Smoky Mountains Study (GSMS) involving children aged nine to 16 were employed.

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Prenatal Smoking and Age at Menarche
Behie, A. M., and M. H. O'Donnell. “Prenatal Smoking and Age at Menarche: Influence of the Prenatal Environment on the Timing of Puberty.” Human Reproduction, vol. 30, no. 4, Oxford University Press, 2015, pp. 957–62, doi:10.1093/humrep/dev033.

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Dubas J S, Baenninger M, Newcombe, Nora, Dubas, Judith Semon, and Baenninger, MaryAnn. “Associations of Timing of Puberty, Spatial Ability, and Lateralization in Adult Women.” Child Development. 60, no. 1 (1989): 246–54. https://doi.org/10.2307/1131089.

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Abstract

Background. Children are commonly exposed at background levels to several ubiquitous environmental pollutants, such as lead and persistent organic pollutants, that have been linked to neurologic and endocrine effects. These effects have prompted concern about alterations in human reproductive development. Few studies have examined the effects of these toxicants on human sexual maturation at levels commonly found in the general population, and none has been able to examine multiple toxicant exposures. The aim of the current investigation was to examine the relationship between attainment of menarche and levels of 6 environmental pollutants to which children are commonly exposed at low levels, ie, dichlorodiphenyldichloroethylene ( p, p ′-DDE), hexachlorobenzene (HCB), polychlorinated biphenyls (PCBs), mirex, lead, and mercury.

Methods. This study was conducted with residents of the Akwesasne Mohawk Nation, a sovereign territory that spans the St Lawrence River and the boundaries of New York State and Ontario and Quebec, Canada. Since the 1950s, the St Lawrence River has been a site of substantial industrial development, and the Nation is currently adjacent to a US National Priority Superfund site. PCB, p, p′-DDE, HCB, and mirex levels exceeding the US Food and Drug Administration recommended tolerance limits for human consumption have been found in local animal species. The present analysis included 138 Akwesasne Mohawk Nation girls 10 to 16.9 years of age. Blood samples and sociodemographic data were collected by Akwesasne community members, without prior knowledge of participants' exposure status. Attainment of menses (menarche) was assessed as present or absent at the time of the interview. Congener-specific PCB analysis was available, and all 16 PCB congeners detected in >50% of the sample were included in analyses (International Union of Pure and Applied Chemistry numbers 52, 70, 74, 84, 87, 95, 99, 101 [+90], 105, 110, 118, 138 [+163 and 164], 149 [+123], 153, 180, and 187). Probit analysis was used to determine the median age at menarche for the sample. Binary logistic regression analysis was used to determine predictors of menarcheal status. Six toxicants ( p, p′-DDE, HCB, PCBs, mirex, lead, and mercury) were entered into the logistic regression model. Age, socioeconomic status (SES), and BMI were tested as potential cofounders and were included in the model at P < .05. Interactions among toxicants were also evaluated.

Results. Toxicant levels were measured in blood for this sample and were consistent with long-term exposure to a variety of toxicants in multiple media. Mercury levels were at or below background levels, all lead levels were well below the Centers for Disease Control and Prevention action limit of 10 μg/dL, and PCB levels were consistent with a cumulative, continuing exposure pattern. The median age at menarche for the total sample was 12.2 years. The predicted age at menarche for girls with lead levels above the median (1.2 μg/dL) was 10.5 months later than that for girls with lead levels below the median. In the logistic regression analysis, age was the strongest predictor of menarcheal status and SES was also a significant predictor but BMI was not. The logistic regression analysis that corrected for age, SES, and other pollutants ( p, p′-DDE, HCB, mirex, and mercury) indicated that, at their respective geometric means, lead (geometric mean: 0.49 μg/dL) was associated with a significantly lower probability of having reached menarche (β = −1.29) and a group of 4 potentially estrogenic PCB congeners (E-PCB) (geometric mean: 0.12 ppb; International Union of Pure and Applied Chemistry numbers 52, 70, 101 [+90], and 187) was associated with a significantly greater probability of having reached menarche (β = 2.13). Predicted probabilities at different levels of lead and PCBs were calculated on the basis of the logistic regression model. At the respective means of all toxicants and SES, 69% of 12-year-old girls were predicted to have reached menarche. However, at the 75th percentile of lead levels, only 10% of 12-year-old Mohawk girls were predicted to have reached menarche; at the 75th percentile of E-PCB levels, 86% of 12-year-old Mohawk girls were predicted to have reached menarche. No association was observed between mirex, p, p ′-DDE, or HCB and menarcheal status. Although BMI was not a significant predictor, we tested BMI in the logistic regression model; it had little effect on the relationships between menarcheal status and either lead or E-PCB. In models testing toxicant interactions, age, SES, lead levels, and PCB levels continued to be significant predictors of menarcheal status. When each toxicant was tested in a logistic regression model correcting only for age and SES, we observed little change in the effects of lead or E-PCB on menarcheal status.

Conclusions. The analysis of multichemical exposure among Akwesasne Mohawk Nation adolescent girls suggests that the attainment of menarche may be sensitive to relatively low levels of lead and certain PCB congeners. This study is distinguished by the ability to test many toxicants simultaneously and thus to exclude effects from unmeasured but coexisting exposures. By testing several PCB congener groupings, we were able to determine that specifically a group of potentially estrogenic PCB congeners affected the odds of reaching menarche. The lead and PCB findings are consistent with the literature and are biologically plausible. The sample size, cross-sectional study design, and possible occurrence of confounders beyond those tested suggest that results should be interpreted cautiously. Additional investigation to determine whether such low toxicant levels may affect reproduction and disorders of the reproductive system is warranted.

METHODS

Setting

The study was conducted with residents of the Akwesasne Mohawk Nation. The Nation is a sovereign territory lying on both sides of the St Lawrence River and spanning the boundaries of New York State and Ontario and Quebec, Canada. Since the 1950s, the St Lawrence River has been a site of substantial industrial development. Today, several industrial complexes are in close proximity to Akwesasne, including a US National Priority Superfund site (General Motors Central Foundry Division) and 2 New York State Superfund sites (Reynolds Metal Company and Aluminum Company of America). Exposure assessment studies in the 1990s found some local animal species to have PCB, p, p ′-DDE, HCB, and mirex levels above the US Food and Drug Administration human consumption tolerance limits. Current levels of POPs in this study sample of 10- to 16.9-year-old participants largely reflect prenatal and lactational exposure that is consistent with known levels of contaminants among adult women, attributable to past maternal consumption of locally caught, contaminated fish. The history of local environmental pollution, the traditional reliance on locally caught fish and game, and the concerns of community members about the health effects of environmental pollutants prompted human health studies at Akwesasne, including an investigation of adolescent development.

Participants

The study participants, recruitment and data collection protocols, laboratory analysis methods, and substitution methods for toxicant levels below the laboratory minimum detection limits were previously described in detail. Briefly, all data were collected by Akwesasne community members, without prior knowledge of participants' exposure status. All study protocols were approved by the institutional review board at the University at Albany, State University of New York, and informed consent was obtained from all participants. The target population was defined as residents of Mohawk households located in the Akwesasne Mohawk Nation and in neighboring communities within 10 miles of Akwesasne. Of the households meeting the eligibility requirements for the study, 294 mother/adolescent pairs enrolled in the study. Of these, 19 were lost to follow-up, 1 was found to be ineligible, and 3 had blood samples that were broken in transit, for a final sample size of 271 (140 females and 131 males). Of the 140 eligible female participants who finished the study, 138 had complete data for this analysis.

Data Collection and Variables

Menarche

Menarche was measured as present or absent, based on self-report at the time of the interview and blood sample collection.

Socioeconomic Status

A weighted index of socioeconomic status (SES) was created in consultation with Native American informants from the community. The index used data from interviews with mothers and included: employment, marital status, education, house size and condition, number of motor vehicles, and age of newest motor vehicle.

Pollutants

Fasting blood specimens were collected at first rising by trained Mohawk staff members. Toxicants analyzed were lead, mercury, PCBs, p, p′-DDE, HCB, and mirex. Analyses of PCBs and organochlorine pesticides were conducted at the University at Albany School of Public Health Analytical Laboratory. High-resolution, ultratrace, congener-specific analysis was performed with parallel dual-column (splitless injection) gas chromatography with electron capture detection. This method quantitates up to 83 individual PCB congeners and 18 PCB congeners as pairs and triplets, as well as p, p ′-DDE, HCB, and mirex. Lead and mercury analyses were conducted by Le Centre de Toxicologie due Quebec (Sainte-Foy, Quebec, Canada). Mercury analysis was based on cold-vapor atomic absorption spectrometry. Lead was analyzed with Zeeman-corrected graphite furnace atomic absorption spectrometry.

The US Environmental Protection Agency recommended method was used to impute values below the minimum detection limits for lead, mercury, PCBs, and HCB, all of which had rates of detection of ≥50%. Lead, mercury, PCBs, p, p ′-DDE, and HCB were natural-logarithmically transformed, because of the skewness of the toxicants. Mirex levels were categorized into 3 groups because of the high rate of undetectable levels, ie, nondetects (below the minimum detection limit of 0.02 ppb; 51.4% of the sample), low detects (0.02-0.03 ppb; 20.3% of the sample), and high detects (0.04-1.17 ppb; 28.3% of the sample).

We considered the 16 PCB congeners with a >50% rate of detection in our sample for hypothesis testing. Three representations of PCB burden were tested, on the basis of the PCB congener groups described by Wolff and co-workers, ie, estrogenic/neurotoxic, antiestrogenic/dioxin-like, and enzyme-inducing (Table 1).

Statistical Analyses

We used probit and logistic regression to model the probability that study participants reported the presence (scored 1) or absence (scored 0) of menarche and how that probability was altered by changes in relevant independent variables. The motivation for both models can be found in the generalized linear model approach to describing models of binary outcomes. The cumulative distribution functions of the probit and logistic regression models are quite similar and generate predicted probabilities that are almost identical. The choice is often dictated by disciplinary preference rather than inferential properties. We used the probit model to estimate the median age at menarche but we used logistic regression to interpret the effects of toxicants on the attainment of menarche, because of its greater flexibility in describing model results.

The median age at menarche was estimated to establish the comparability of the sample to other populations, as well as to compare the effect of high versus low lead levels on age at menarche without adjustment for additional toxicants or covariates. The median age at menarche for the sample was estimated with probit analysis using the status quo method. With the status quo method, age and the presence or absence of menarche are assessed at the time of the interview. The combination of probit analysis and the status quo method is the best method for estimating the median age at menarche for a population, because it eliminates recall bias and solves the problem posed by individuals who have not yet reached menarche. Instead of recall of the age at menarche, the probit transformation is applied to the distribution of the percentage of postmenarcheal girls in each age group. The age corresponding to 50% of the probit distribution is the predicted median age at menarche for the population.

Binary logistic regression analysis was used to test the influence of 6 toxicants (mirex, p, p′-DDE, HCB, PCBs, lead, and mercury) on the likelihood (log odds) of having attained menarche (yes/no), controlling for other influences on menarche. The control variables (age, SES, and BMI) tested for inclusion in the model were retained in the model if they reached statistical significance ( P < .05). Any variable not included on the basis of statistical significance was reconsidered, to estimate the effects on results and to determine whether its exclusion would alter any observed effects of toxicants. All continuous independent variables were mean-centered. Squared terms were included to test for nonlinear effects. All statistical testing was performed with SPSS software, version 11.5.0 (SPSS, Chicago, IL). An α level of .1 was chosen for inclusion of nonlinear terms. An α level of .05 was used for testing of all other effects. Squared terms that were maintained in the model and their corresponding variable main effects were tested at several toxicant levels.

In addition, a logistic regression model with age, SES, and only 1 toxicant was run for each toxicant. We compared the results of the single-toxicant models with the model containing all 6 toxicants simultaneously. The purpose of this comparison was to test the influence of additional toxicants in the multiple-toxicant model on the observed effect of a given toxicant.

RESULTS

Toxicant Levels

Toxicant levels for this sample of Mohawk girls are shown in Table 2. Levels were consistent with long-term exposure to a variety of toxicants in multiple media. Mercury levels in the current study were at or below background levels observed for the general population (0.1-0.8 μg/dL). The highest lead level was less than one half the Centers for Disease Control and Prevention action limit of 10 μg/dL. PCB levels were consistent with a pattern of both cumulative and recent exposure.

Probit Analysis

Girls included in this analysis ranged in age from 10 through 16.9 years; 83 (59.7%) had reached menarche. With probit analysis, the median predicted age at menarche for the total sample was 12.2 years (95% confidence interval: 11.9-12.5 years). This group of Mohawk girls was comparable to a larger sample of 10- to 16-year-old American girls from the Third National Health and Nutrition Examination Survey (NHANES III), in terms of the distribution of menarcheal status according to age (Table 3).

Girls at or above the median blood lead level of 1.2 μg/dL had a predicted age at menarche of 12.7 years (95% confidence interval: 12.2-13.1 years), without adjustment for any other factors that can influence age at menarche. Girls below the median lead level had a predicted age at menarche of 11.8 years (95% confidence interval: 9.9-12.8 years), 10.6 months earlier than that for girls with higher lead levels.

Logistic Regression

Binary logistic regression analysis predicting menarcheal status (premenarcheal or postmenarcheal) was used to consider simultaneously the effects of multiple toxicants while controlling for other influences on menarche (Table 4). The effect associated with each predictor variable takes into account all other variables in the model. As expected, age was the strongest predictor of attainment of menarche in the binary logistic regression analysis and was positively associated with having reached menarche. Lower SES was related to higher odds of having reached menarche. In other words, same-aged girls with lower SES were more likely to have reached menarche than were girls with higher SES. Mirex, p, p′-DDE, and HCB were unrelated to menarcheal status. The effect of BMI was tested, but BMI was found not to be a significant predictor in the model, perhaps because of its association with age ( r = 0.322, P < .001), which is included in the model.

A nonlinear effect was observed for lead, as indicated by the squared term in Table 4. At the geometric mean (0.49 μg/dL) and 75th percentile (1.66 μg/dL), lead was associated with a lower likelihood of having attained menarche, after adjustment for age, SES, and other toxicants. This main effect of lead was not significant below the geometric mean. A 100% increase in lead levels above the mean, from 0.49 to 0.98 μg/dL, decreased the odds of reaching menarche by 72% when all other variables were held constant at their respective means. The odds of reaching menarche decreased by 98% with a doubling of lead levels above the 75th percentile, from 1.66 to 3.32 μg/dL.

The estrogenic PCB (E-PCB) group described by Wolff and co-workers was associated with a higher likelihood of having reached menarche, after adjustment for age, SES, and other toxicants. A 100% increase in E-PCB levels above the mean, from 0.12 to 0.24 ppb, was associated with 8.4 times greater odds of having reached menarche. Using the same logistic regression analytic technique, we tested the effects of the 2 other classes of PCBs (antiestrogenic and enzyme-inducing) described by Wolff and co-workers. No relationship was observed between menarche and the PCB groups that Wolff and co-workers classed as antiestrogenic or enzyme-inducing.

A nonlinear effect of mercury was observed, as indicated by the squared term in Table 4. The main effect of mercury was not significant at the mean and was marginally significant (β = 2.57, P = .08, 2-tailed test; results not shown) at the geometric 95% percentile of mercury levels (0.28 μg/dL).

Figures 1 and 2 show predicted probabilities of 12-year-old Mohawk girls reaching menarche at the geometric mean lead level and above (Fig 1) and at all levels of E-PCB (Fig 2), controlling for age, SES, and all other toxicants. Predicted probabilities for lead are not shown below the geometric mean because lead was a significant predictor of menarcheal status only at the geometric mean and above. Calculations were based on the mean-centered logistic regression model presented in Table 4, with all other variables held constant at their respective means. Approximately 69% of 12-year-old girls were predicted to have reached menarche. As lead levels increased to the 75th percentile, 10% of 12-year-old Mohawk girls were predicted to have reached menarche. As the levels of E-PCB increased, the predicted probability of 12-year-old Mohawk girls having reached menarche increased from 52% at the 25th percentile of E-PCB levels to 69% at the mean and to 86% at the 75th percentile.

To substantiate the interpretation of coefficients in the logistic regression model containing all 6 toxicants (Table 4), single-toxicant logistic regression models that corrected only for age and SES were considered. We compared these single-toxicant models with the model shown in Table 4 and found little change in the measure of effect (β coefficients), with the exception of mercury (results not shown). Neither main nor nonlinear effects of mercury were found in the model containing only age, SES, and mercury. Also, adding BMI to the logistic regression model (Table 4) had little effect on the relationships between menarche and either lead or E-PCB, as indicated by the small changes in β coefficients (lead: without BMI, β = −1.29; with BMI, β = −1.10; E-PCB: without BMI, β = 2.13; with BMI, β = 1.98).

We assessed nonadditivity in the effects of toxicants in the 6-toxicant model. Interactions among all pairs of the 6 toxicants were tested. Three statistically significant interactions were detected, namely, lead and E-PCB, lead and HCB, and lead and mirex (results not shown). In the 3 models with significant interaction terms, age, SES, E-PCB, and lead remained significant at P < .05. To estimate how the effects of toxicants were conditioned by levels of the other toxicants, predicted probability plots were compared, those based on the presented model without interactions (Table 4) and those based on models including interactions. The patterns of effects for each toxicant were indistinguishable across models.

DISCUSSION

Analysis of multichemical exposure among Akwesasne Mohawk adolescent girls provides evidence that lead and certain PCB congeners may affect attainment of menarche. These associations were observed after controlling for potential confounders. No association was observed between mirex, p, p ′-DDE, or HCB and menarcheal status.

In this study, lead was associated with a later median predicted age at menarche, without controlling for other variables, as well as a reduced likelihood of having reached menarche, controlling for other toxicants, age, and SES. This finding is consistent with analyses of the NHANES III data that showed 1- to 6-month delays in attainment of menarche and Tanner breast and pubic hair stages among girls 8 to 18 years of age with only modest increases in blood lead levels from 1 to 3 μg/dL. The NHANES III effects were seen after adjustment for socioeconomic factors and body size, which suggests that lead might have delayed maturation through changes in the endocrine system, rather than as a consequence of delayed growth. Although the effect we observed was larger, it was stable across analyses, both with and without control for SES, BMI and other toxicants. One possible explanation for the larger effect size is our greater control for other toxicant levels, which could have maximized the observed effect of lead.

The plausibility of the observed relationships between higher lead levels and a lower likelihood of having reached menarche and delayed menarche is supported by animal studies showing that lead exposure delayed pubertal development and reduced reproductive organ growth. Two biological mechanisms might be at work here. Lead might alter sexual maturation through direct effects on all levels of the hypothalamic-pituitary-gonadal axis. Lead might also indirectly affect sexual maturation by restricting or delaying growth. Several cross-sectional studies found higher lead levels to be associated with decreased weight and height. Body size, in turn, has been directly related to the timing of sexual maturation.

In addition to the effect of lead, a group of 4 potentially estrogenic PCB congeners was found to be associated with a greater likelihood of having attained menarche, controlling for age, SES, lead, mercury, p, p′-DDE, HCB, and mirex. Few other studies are available for comparison, and among these there is some variation in results. Among breastfed girls, perinatal polybrominated biphenyl exposure was associated with earlier pubic hair staging, and in utero polybrominated biphenyl exposure was associated with earlier menarche. Similarly, significantly higher concentrations of p, p ′-DDE were found among girls with precocious puberty who immigrated to Belgium from developing countries. Among girls in a North Carolina cohort, there was some evidence that PCB exposure was associated with younger ages at attainment of pubertal stages, but results were not conclusive because of the small sample size. These associations of POP exposure with earlier sexual maturation are consistent with the present study. However, a study of Flemish adolescents found an association between dioxin-like compounds and delayed attainment of Tanner adult breast stage, and neither PCB levels nor polychlorinated aromatic hydrocarbon exposure was significantly correlated with the timing of menarche or pubic hair staging among girls. These differences in results (delay, acceleration, or no effect) might be attributable to exposure to different types and/or combinations of POPs, which can have estrogenic, androgenic, and antiestrogenic effects. In addition, some of these studies focused on 1 or 2 toxicants or classes of toxicants in their analyses, leaving open the possibility that other covarying but unmeasured toxicants modify the observed effects.

PCBs and related compounds have been associated with several other effects related to the reproductive system, including decreased implantation rate, litter size, and sexual receptivity among animals, as well as reduced fecundity, menstrual irregularity, decreased sperm motility, and hormonal changes among humans. Although these effects are consistent with our results, the exact mechanisms underlying the effects of POPs are unclear. Furthermore, >1 pathway may be involved, depending on the combination, concentration, and timing of POP exposure, as well as the species affected. Although the specific mechanisms of effects are not known, modification of the hypothalamic-pituitary-gonadal axis has been proposed as a likely means of action.

The results for mercury reported here cannot be assessed against other research because no investigations of the relationship between mercury levels and sexual maturation among humans have been published. Animal studies indicate the possibility of endocrine and reproductive effects of mercury.

The relationship observed here between lower SES and earlier menarche requires interpretation. Higher SES has been shown to be associated with earlier menarche. However, this negative relationship was observed in settings in which nutritional status is highly variable and strongly related to socioeconomic factors. Other studies that found no relationship involved well-off populations without threats to maturation from nutritional stress. The Akwesasne Mohawk sample demonstrates no evidence of nutritional deficiency that would affect menarche, and the observed relationship between menarche and SES fits the pattern observed for well-off samples.

Here our focus was not on the relationship of SES to menarche but on the role of SES in influencing the relationship of lead and PCBs to menarche. In the present study, the removal of SES from the logistic regression model had little impact on the effects of age and toxicants on menarche (on the basis of changes in β coefficients) or on the pseudo-variance explained (2.8% reduction in both Cox-Snell and Nagelkerke pseudo- R ²).

This study is distinguished by its ability to consider multiple common toxicants simultaneously and to include congener-specific PCB analysis. Despite relatively low toxicant levels in our sample, both lead and E-PCB were found to be associated with attainment of menarche after controlling for age, SES, and other toxicants. By testing several PCB congener groupings, we were able to determine that specifically a group of potentially estrogenic PCB congeners affected the odds of reaching menarche. Although a nonlinear effect of mercury on menarche was suggested, with the effect strengthening at higher levels, mercury did not reach statistical significance in our model. Additional tests of single-toxicant models suggested that the results observed for lead and E-PCB were robust and not influenced by the other model variables, as indicated by the stable β coefficients. Body size had little impact on the associations of lead or E-PCB levels with menarcheal status in this sample. Inclusion of terms representing interactions among the toxicants did not substantially change the effects of each toxicant. The small sample size and very small number of participants at the extremes of the interaction space limit our ability to generalize from analyses of interactions.

CONCLUSIONS

We observed an association between low levels of 4 potentially estrogenic PCB congeners and lead and the attainment of menarche, controlling for SES, age, and other toxicants. These findings are consistent with the literature and are biologically plausible. However, cautious interpretation is warranted because of the sample size, the cross-sectional study design, and the possible occurrence of confounders beyond those tested, including genetic factors. In this, as in other observational studies, the results are derived from a specific range of values, and it is inappropriate to generalize the effects to levels above or below the values in this sample. At much higher or lower levels of lead and/or PCBs, different effects may occur. Findings reported here suggest that the timing of sexual maturation may be sensitive to relatively low levels of lead and certain PCB congeners. Additional investigation to determine whether such low levels may affect reproduction and disorders of the reproductive system is warranted.

Acknowledgments

This work was supported by grants from the National Institute of Environmental Health Sciences (grants ES04913-09, ES07231-07, and ES10904-05).

We thank the Akwesasne Mohawk community for their cooperation and participation in this research and Dr David O. Carpenter for his leadership in the Superfund Basic Research Program at the University at Albany, State University of New York.

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Relationship of Lead, Mercury, Mirex, Dichlorodiphenyldichloroethylene, Hexachlorobenzene, and Polychlorinated Biphenyls to Timing of Menarche Among Akwesasne Mohawk Girls

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Background. Children are commonly exposed at background levels to several ubiquitous environmental pollutants, such as lead and persistent organic pollutants, that have been linked to neurologic and endocrine effects. These effects have prompted concern about alterations in human reproductive development.

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Louis, G. M. B., Gray, L. E., Marcus, M., Ojeda, S. R., Pescovitz, O. H., Witchel, S. F., ... & Bourguignon, J. P. (2008). Environmental factors and puberty timing: expert panel research needs. Pediatrics, 121(Supplement 3), S192-S207.

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Nick Piedad (Genes link puberty timing to body fat in women)

# data[].attributes.subject
Nick Piedad (Genes link puberty timing to body fat in women)

# data[].attributes.body
Boston University Medical Center. (2010, November 22). Genes link puberty timing to body fat in women. ScienceDaily. Retrieved September 11, 2019 from www.sciencedaily.com/releases/2010/11/101121160234.htm

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Genes link puberty timing to body fat in women -- ScienceDaily

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Genetic and Environmental Influences on Pubertal Timing Assessed by Height Growth

Wehkalampi, K., Silventoinen, K., Kaprio, J., Dick, D. M., Rose, R. J., Pulkkinen, L., & Dunkel, L. (2008). Genetic and environmental influences on pubertal timing assessed by height growth. American journal of human biology : the official journal of the Human Biology Council, 20(4), 417–423. doi:10.1002/ajhb.20748

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Savannah Nguyen                                  Puberty and Influencing Factors in Schoolgirls Living in Istanbul: End of the Secular Trend?  

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Savannah Nguyen                                  Puberty and Influencing Factors in Schoolgirls Living in Istanbul: End of the Secular Trend?  

# data[].attributes.body
Zeynep Atay, Serap Turan, Tulay Guran, Andrzej Furman, and Abdullah Bereket. 2011. Puberty and Influencing Factors in Schoolgirls Living in Istanbul: End of the Secular Trend? (July 2011). doi:10.1542/peds.2010-2267

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Does Vitamin D affect timing of menarche?
Anna Chew and Susan S Harris
Chew, A., & Harris, S. S. (2013). Does vitamin D affect timing of menarche? Nutrition Reviews, 71(3), 189–193. https://doi.org/10.1111/nure.12015

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Does vitamin D affect timing of menarche?

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Earlier Onset of Puberty in Girls: Relation to Increased Body Mass Index and Race

Paul B. Kaplowitz, MD, PhD*; Eric J. Slora, PhD‡; Richard C. Wasserman, MD, MPH‡§;
Steven E. Pedlow, BSi; and Marcia E. Herman-Giddens, PA, DrPH¶

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Father Absence and Accelerated Reproductive Development in Non-Hispanic White Women in the United States.

Gaydosh L, Belsky D, Domingue W, Boardman B, Harris J. Father Absence and Accelerated Reproductive Development in Non-Hispanic White Women in the United States. Demography. 2018;55(4):1245-1267. doi:10.1007/s13524-018-0696-1

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Phthalates may promote female puberty by increasing kisspeptin activity
Chen et al. 2013. Human Reproduction Vol. 28(10): 2765-2773.

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Phthalates may promote female puberty by increasing kisspeptin activity

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Socio-Environmental Factors Associated with Pubertal Development In Females: The Role of Pre-Pubertal Tobacco and Alcohol Use
Jennifer David Peck
Peck, J. D., Peck, B. M., Skaggs, V. J., Fukushima, M., & Kaplan, H. B. (2011). Socio-environmental factors associated with pubertal development in female adolescents: the role of prepubertal tobacco and alcohol use. The Journal of adolescent health : official publication of the Society for Adolescent Medicine, 48(3), 241–246. doi:10.1016/j.jadohealth.2010.06.018

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SOCIOENVIRONMENTAL FACTORS ASSOCIATED WITH PUBERTAL DEVELOPMENT IN FEMALES THE ROLE OF PREPUBERTAL TOBACCO AND ALCOHOL USE

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Associations between early alcohol and tobacco use and prolonged time to puberty in boys

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SOCIAL FACTORS AFFECTING THE ONSET OF PUBERTY
Smith, P. K., & Alsaker, F. (1999). Social factors affecting the onset of puberty. Journal of Reproductive and Infant Psychology, 17(2), 109–110. https://doi.org/10.1080/02646839908409090

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Section:

SPECIAL FEATURE

EDITORIAL

The first three papers of this issue make up a special feature examining the social factors that affect the onset of puberty. Such factors may include family composition, interpersonal relationships with parents and/or peers, family stress and experience of sexual abuse, the cultural and historical context, and perceptions of puberty as mediated by the social environment (Alsaker, 1995).

The negative impact on pubertal development of factors such as inadequate nutrition has been well documented. The finding that less well fed young people delay puberty is understandable from both a causal viewpoint and in terms of a developmental pathway in which it is inadvisable to enter the stressful and energy-consuming changes of puberty when the body is not physically well prepared to do so. However, the impact of social factors is less well documented, and certainly less well understood. An important theoretical contribution, and one which all three papers here refer to, has been that of Belsky et al. (1991). Building on work suggesting that father absence was associated with earlier puberty, they proposed a life-span approach envisaging different developmental pathways. One pathway involved secure, non-stressful family relationships, later puberty and more discriminate and stable sexual behaviour. Another pathway involved less secure and more stressful relationships, earlier puberty, and less discriminate sexual behaviour. In effect, the child's early family experiences were assumed to give an indication of the kinds of resource situation and relationship quality that the child might experience later, with their adolescent reproductive strategy being adjusted accordingly. Links can be made between this approach and ideas from evolutionary theory, especially life history theory (e.g. Stearns, 1992) and related ideas in attachment theory (e.g. Chisholm, 1996).

For this special feature, four papers were submitted, and three accepted (the paper by Kim & Smith was dealt with entirely by Alsaker). The three papers cover samples from different countries and use different methods, but all bear on the topic of puberty focusing particularly on the model of Belsky et al. (1991).

Turner, Runtz and Galambos report data from Canada, in which experience or not of sexual abuse is related to pubertal development. The clear finding is that sexual abuse is related to early puberty, despite matching of groups for many demographic and socio-economic characteristics. The finding of earlier puberty in sexually abused girls is quite consonant with the Belsky et al. (1991) model, although there remain obvious questions about mechanism; could early puberty bring greater risk of sexual abuse, for example, rather than vice versa? Another interesting finding was that sexually abused girls felt subjectively older, but this effect was not mediated by pubertal timing. This study has a small sample, as is often characteristic for studies with clinical populations.

Hulanicka, by contrast, reports data from large samples. She reports on a number of studies of factors affecting puberty in Poland. Her research summary covers several studies, results of which are not readily available in English language journals. These, plus her own studies, clearly show that various family stresses, or what she terms `dysfunctional families', can lead to earlier puberty in girls, despite the often poorer socio-economic status and nutrition of such families. Hulanicka's survey also covers different time points in recent Polish history, and relates findings to the social and historical context of the country. Interestingly, her final regression analyses failed to find an effect of father absence or dysfunctional family on age of puberty, independent of her other factors (her Tables 4 and 5); this suggests that these effects may be mediated by factors such as family size, accommodation, and parental education, or most probably to psychological variables related to these (such as family conflict) which were not directly measured in these large scale studies.

Kim and Smith report on a moderately sized sample from northern England, in which a range of characteristics were measured in both males and females. Although not many significant results were obtained, those that were (such as parental conflict and independence from parents in girls, and emotional distance from mother in boys) are in the direction predicted by Belsky et al. (1991). These results lead to postulated path models linking childhood experiences via pubertal age (menarche or spermarche) to reproductive behaviour as young adults (their Figures 1 and 2). However, the retrospective nature of all their data needs to be born in mind as a limitation of such interpretations.

The three papers illustrate the range of samples, approaches and findings now being used in this area, and the international nature of the research. These and other studies clearly implicate the existence of social factors (as well as physical and nutritional) that affect the age of puberty, in girls and probably also in boys. These factors appear to be related to childhood stress. However, the precise indicators vary in different studies, and causal relationships are unclear. Longitudinal studies will be necessary for further progress here in helping to disentangle what may be a very complex network of relationships, in which the cultural and historical context of the studies must be fully recognized.

Address for correspondence: Professor Peter K. Smith, Department of Psychology, Goldsmiths College, New Cross, London SE16 6NW, UK. Professor Francoise Alsaker is at the University of Bern, Switzerland.

ALSAKER, F.D. (1995). Timing of puberty and reactions to pubertal changes. In: M. RUWFER (Ed.), Psychosocial disturbances in young people: challenges for prevention (pp. 37-82). New York: Cambridge University Press.

BELSKY, J., STEINBERG, L. & DRAPER, P. (1991). Childhood experience, interpersonal development, and reproductive strategy: an evolutionary theory of socialization. Child Development, 62, 647-670.

CHISHOLM, J. (1996). The evolutionary ecology of attachment organisation. Human Nature, 7, 1-38.

STEARNS, S. (1992). The evolution of life histories. New York: Oxford University Press.

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By P. K. Smith and F. Alsaker

This article is copyrighted. All rights reserved. Source: Journal of Reproductive & Infant Psychology

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Social factors affecting the onset of puberty

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Section: SPECIAL FEATURE EDITORIAL The first three papers of this issue make up a special feature examining the social factors that affect the onset of puberty. Such factors may include family composition, interpersonal relationships with parents and/or peers, family stress and experience of sexual abuse, the cultural and historical context, and perceptions of puberty as mediated by the social environment (Alsaker, 1995).

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Environmental and genetic pathways between early pubertal timing and dieting in adolescence: distinguishing between objective and subjective timing

Harden, K. P., Mendle, J., & Kretsch, N. 2012. Psychological Medicine Vol. 42(1):183–193. doi:10.1017/S0033291711000961

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Genetic and environmental influences on pubertal timing assessed by height growth
Wehkalampi et al. 2008. American Journal of Human Biology Vol. 20(4):417-423.

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Beyond overweight: nutrition as an important lifestyle factor

influencing timing of puberty

Cheng et al. 2012. Nutrition Reviews Vol. 70(3):133–152.

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Association of phthalates, parabens, and phenols found in personal care products with pubertal timing in girls and boys
Harley et al. 2018. Human Reproduction Vol. 34(1): 109-117.

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Association of phthalates, parabens, and phenols found in personal care products with pubertal timing in girls and boys