COMMENTARY |
Navigating the Recent Articles on Girls’ Puberty in Pediatrics: What Do We Know and Where Do We Go from Here?
Department of Maternal and Child Health
School of Public Health
University of North Carolina
Chapel Hill, NC 27599
North Carolina Child Advocacy Institute
Raleigh, NC 27601
Department of Pediatrics
Virginia Commonwealth University School of Medicine
Richmond, VA 23298
Pediatric Research in Office Settings
Center for Child Health Research
American Academy of Pediatrics
Elk Grove Village, IL 60007
Department of Pediatrics
University of Vermont College of Medicine
Burlington, VT 05405
Abbreviations: PROS, Pediatric Research in Office Settings • NHANES, National Health and Nutrition Examination Survey • NHES, National Health Examination Survey
After the publication of the Pediatric Research in Office Settings (PROS) study on the age of onset of pubertal characteristics and menses in US girls in 1997,1 a spate of related articles have appeared on emerging questions and controversies over recent pubertal data and the implications of these findings for clinical practice. The purpose of this commentary is to 1) summarize the consistencies and contradictions among some of these newer communications, 2) address misconceptions and misinterpretations of the PROS data, and 3) identify legitimate points of disagreement and areas for additional investigation.
A survey of just some of the recent articles demonstrates the scope of additional research both in our country and abroad.2–17 The 1997 PROS study, a convenience sample of 17 077 white and black girls seen in pediatric practices across the United States and Puerto Rico used the Tanner method18 to describe the ages of onset of breast development, pubic hair growth, and menarche. It found that the mean ages for these characteristics varied significantly between white and black girls (with black girls being at younger ages), the median age of menarche for black girls had dropped over the past several decades, and the ages for the onset of development seemed to be earlier than previous US studies as well as Marshall and Tanner’s classic 1969 study.18 The PROS study pointed out that the prevalence of secondary sexual characteristics in girls <8 years old was substantially higher than what had been believed previously and "that more appropriate standards for defining delayed and precocious puberty may need to be developed, that the timing of sex education in the schools may need revision, and that the etiology and effects require further study." The authors stated, "The findings of this study need to be confirmed in other research including a nationally representative sample such as HANES [Health and Nutrition Examination Survey]."1 After the PROS study, Kaplowitz et al2, using its data, provided additional analyses and new recommendations calling for the age for referral for precocious puberty to be lowered.
Between October 2002 and April 2003, Pediatrics alone has published 10 articles on puberty markers or issues.19–28 Several of these articles beg for comment, in particular the articles that propose changes in practice or present interpretations of findings that contradict those of other recent articles. Six of the articles have been based wholly or in part on the most recent National Health and Nutrition Examination Survey (NHANES) data, and some present overlapping results or conflicting conclusions.20,21,23–25,28
The October 2002 article by Wu et al20 analyzed data from the NHANES to report on ethnic differences in secondary sexual characteristics and menarche. The authors presented mean ages of onset for breast and pubic hair growth and for menses by race and ethnicity as well as odds ratios of having attained pubertal milestones among the 3 racial/ethnic groups studied in the NHANES. Tables 1 and 2 compare these results with those of the PROS study1 and the analyses of the NHANES data for average ages of onset of breast and pubic hair growth and menses by Sun et al24 and Chumlea et al25, respectively. Age at menarche was estimated by Wu et al by both the status quo method as well as an estimate based on the self-reported age using a failure time model, both under the assumption of a normal distribution of the event (Table 2). Their mean ages for menarche differ slightly from those of the Chumlea et al analysis (see below) of the NHANES data published in January 2003 because of different statistical methods. Wu et al concluded that black girls enter puberty earliest, followed by Hispanic and then white girls. Numerous studies, including the 1997 PROS study, have found earlier puberty among black girls. The Wu et al analysis provides the important additional information that racial and ethnic differences among the NHANES populations are independent of select social and economic factors.
|
|
In the same issue of Pediatrics, the article by Freedman et al22 looked at the relation of age at menarche to race, time period, and anthropometric dimensions by using the Louisiana population followed in the Bogalusa Heart Study. Their assessment of secular trends in menarcheal age between 1973 and 1994 found that the mean menarcheal age decreased by 9.5 months for black girls and 2 months for white girls over the 20-year time period. As in other studies, they also found that black girls matured earlier than white girls.
The November 2002 article by Sun et al, "National Estimates of the Timing of Sexual Maturation and Racial Differences Among US Children,"24 used NHANES data to look at ages at entering a sexual maturity stage as well as being in the stage for both boys and girls and by race and ethnic groups, whereas the Wu et al20 article reported only on mean ages at entering a stage (Tables 1 and 3). As would be expected, the results of these 2 articles are very similar, and the authors stressed that the degree of racial differences requires separate normative reference data, a recommendation with which we agree.
|
The NHANES data support the findings of the PROS study and, for the most part, show close or similar results, although the PROS population was a convenience sample of girls being seen in pediatric practices across the country, as compared with the nationally representative population sample from the NHANES. Examination of Table 3 shows confidence intervals from the PROS data overlapping proportions from the NHANES data in a number of cells. Where results are not overlapping, in some cells the NHANES reports a higher proportion by race and age of girls with a particular characteristic than in the PROS study but in others reports a lower proportion (selected and weighted to be nationally representative, sample sizes for breast and pubic hair examination [ages 8–13] for each race and age ranged from 41 to 77 for the NHANES; similarly, the cell ranges for the convenience sample for the PROS study were 91–1334).
Sun et al24 proposed that the results of their NHANES analysis provide "normative reference data." Although we are focusing our comments on girls, this recommendation with regard to boys especially should be questioned, given the very young ages at which 25% of all US boys were found to have begun puberty (
8 years old) and the lack of any discussion about data quality.
Several statements in their article are unclear:
- The authors state that "on average, girls start to mature earlier than boys by approximately 1.5 years," but they do not explain how they came to this conclusion given their finding that (for whites) the median age for onset of breast development in girls was 10.38 years as compared with the age of onset of genital growth for boys, which was 10.03 years. For pubic hair growth, the median age of onset for white girls and boys was 10.57 and 11.98 years, respectively. Age differences by characteristic were similar for blacks and Mexican Americans. Because breast and genital growth are usually considered better markers for the onset of puberty than pubic hair growth, these NHANES data would indicate that boys begin puberty earlier than girls.
- The article goes on to state that all racial/ethnic groups completed sexual development at "approximately the same ages." The data show that black girls enter stage 5 breast development at 14.0 years and white girls at 15.5 years, and black boys enter stage 5 genital growth at 15.0 years and whites at 16.0. If data for being in a stage are used, black girls are in stage 5 breast development about a half-year earlier than white girls, and black boys are in stage 5 genital development a full year earlier than white boys. Thus, it would seem that a more accurate interpretation of the data are that black girls and boys reached sexual maturity approximately a year earlier than whites.
- The article states that the PROS study "did not include girls older than 13 years, so the contribution of late-maturing girls to the results were not considered." This comment may confuse readers, because the authors do not go on to explain that probit analysis, the statistical method used, has the capability of obtaining estimates from data for which only a portion of subjects have achieved the characteristics being studied (see additional discussion below in the section on the article by Chumlea et al). They would have known this because not only is this stated in the PROS article, but they use the same analytic techniques themselves. In addition, because they were aware that the lack of data from pertinent age groups may bias the analysis, the authors should have stated that the lack of NHANES data on early-maturing girls could have affected age estimates for younger girls’ events; the NHANES did not collect pubertal data until 8 years of age. Of these girls, 6% to 30% (depending on race) already had at least 1 secondary sexual characteristic at the earliest age for which data were collected.
- Because NHANES data are derived from complex, stratified, multistage probability cluster design samples representative of noninstitutionalized US civilians, results of analyses are intended to represent the US population in question. For this reason, the authors propose that their "study presents national reference data for sexual maturation." We would caution against adopting these results without additional discussion and studies. It is important to realize that assessment of breast or genital stages of development in the NHANES study was made by visual inspection only.9 There was no palpation of the breasts in girls or the genitalia in boys. Questions have been raised regarding the accuracy of breast staging without palpation by critics of the PROS study, especially in overweight girls.2,19 If critics question the accuracy of staging breast development without using palpation, then this concern must apply to the NHANES data as well. The accuracy of visual inspection as compared with palpation has been examined in the PROS study but not in the NHANES. PROS clinicians recorded breast development both by Tanner staging and palpation for 39% of the subjects. Analyses of these data for Tanner stage 2 found overrating by inspection in 4% and underrating in 1.7%. Misclassifications were as likely to occur in thinner girls as in more overweight girls; therefore, there was no evidence that the proportion of young girls found to have breast development could be explained by observer error in scoring fat tissue as breast tissue.2
In January 2003, Chumlea et al published "Age at Menarche and Racial Comparisons in US Girls,"25 which also used data from the NHANES study and shares many of the same authors as the previous article. This article repeats the analysis on menarcheal age by the Wu et al20 article, with some differences in technique. The former calculated the average age of onset of menses both using probit and failure time methods, and the latter used the percentage of girls having begun menses during 3-month age groupings in a probit model. Chumlea et al also present their results in a format differing from Wu et al, including probit plots and the ages at which 10%, 25%, 50%, 75%, and 90% of girls by race had reached menarche. As reported by Wu et al, they found that black girls began menses earlier than white and Mexican American girls. Statistically significant racial differences were reported by P values and 95% confidence intervals. The authors calculated a median overall age for onset of menses of 12.43 years of age for NHANES girls and compared it with the overall of age of 12.76 years from the MacMahon29 analysis of the National Health Examination Survey (NHES) conducted 
25 years ago, a difference of 4.0 months. (For the NHANES, "overall" included white, black, and Mexican American girls; for the NHES, "overall" included white and black girls.) The authors concluded that, "overall, US girls are not gaining reproductive potential earlier than in the past." In contrast, the April 2003 article in Pediatrics by Anderson et al28 presented their own analyses of NHES and NHANES menarcheal data, focusing on secular trends and the influence of weight and race on the age of onset of menses. These authors concluded that the average age of menarche had dropped by 0.21 years (2.5 months) during this 25-year time period and that it represented a statistically significant secular trend (Table 2).
Several points in the Chumlea et al article deserve additional comment.
- The PROS study is mentioned in both the introduction and discussion sections; the authors state that the PROS findings are subject to bias, because " 25% of all US girls ... reach menarche after 13 years of age," and the PROS study did not include girls over this age. Although probit analysis has the capability of obtaining estimates from data for which only a portion of subjects have achieved the characteristics being studied, bias is possible, because the technique is most accurate when at least 50% of the subjects have obtained the characteristic in question. The PROS study had only 35.2% of the population at 12 years of age having reached menarche. Nonetheless, under the assumption that the onset of menses follows a normal distribution, estimating the median (mean) age for menarche from the PROS population was valid, although not as precise, given that the proportion with this characteristic was <50%. The confidence intervals for the average age of menarche from the PROS data overlap with those from the NHANES in the Wu et al and Chumlea et al analyses but not those from the Anderson et al results (Table 2). In the PROS population, menarcheal age for black girls, whose menarcheal proportion at 12 years was 62.1%, was virtually identical to that of the NHANES.
- Chumlea et al state, "the median (mean) age at menarche for all US girls has not changed significantly in 30 years with a shift of only 4 months in that period." Given that statement, the question arises as to whether the differences they present in median age between the NHES and NHANES (12.76 vs 12.43 for the total population) is, in fact, statistically different. Table 2 shows the average age of onset of menses as calculated from data from the NHES, PROS, and NHANES studies by various authors. Because of differences in statistical techniques, there are calculated differences in the average menarcheal age of >1 month from the same NHANES data. Nonetheless, in comparing NHES and NHANES data, it can be seen that the differences between the 2 time periods for most cells are statistically significant, because the confidence intervals are not overlapping. Therefore, if the authors’ use of the term "significant" is in a statistical sense, their statements would seem to be in question. If they used the word "significant" as a term denoting importance, one could question the dismissal of the 4- to 5-month drop in age for black girls and the 2.5- to 3-month drop for white girls over a period of 25 years as not being important or not indicating earlier reproductive potential.
Also in the January 2003 Pediatrics issue was the article by Midyett et al, "Are Pubertal Changes in Girls Before Age 8 Benign?"26 This article presented data on 223 patients referred for precocious puberty to Children’s Mercy Hospital in Kansas City, Kansas, during a 5-year period. The patients were picked to include white girls 7 to 8 years old and black girls 6 to 8 years old, because this represents the group that might not have received an endocrine evaluation if the age limits for evaluation proposed in 1999 were followed.2 They found that 105 girls (47%) had both breast and pubic hair and defined this group as having "true precocious puberty." After finding that 12.3% of the patients had other endocrine conditions, most commonly acanthosis nigricans/hyperinsulinism (n = 15) or hypothyroidism (n = 4), the authors recommended that "all girls with any secondary sexual development before 8 years of age deserve at the minimum a bone age assessment and close longitudinal follow-up."
Although the generalizability of the results to all girls in the United States, as the authors advocate, can be questioned as well as certain other aspects of the study, we restrict our comments to the points below.
- Much of what is problematic in this article results from the authors’ erroneous assumption that a girl needs to have both breasts and pubic hair to be considered as having true precocious puberty. Pubic hair growth in girls is related to adrenal androgen production, the regulation of which is independent of the hypothalamic-pituitary-gonadal axis.30 Growth acceleration and increase in breast size over a period of observation are better clinical indicators of activation of the hypothalamic-pituitary-gonadal axis than whether a girl with breasts also has pubic hair. In their discussion of the PROS study, the authors attempt to calculate from the PROS data the true incidence of precocious puberty, pointing out that "only" 1.6% of black girls and 0.4% of white girls 6 to 7 years old had both breast development and pubic hair growth. Additionally, they calculate that there is no statistically significant difference between these 2 groups and declare that there is no "scientific basis" for using separate guidelines for black and white girls. These conclusions are flawed because of the unwarranted assumption that girls with breast tissue but no pubic hair fall into a separate category than girls with only breast tissue. Although not all 6- to 8-year-old girls with breast development have the rapidly progressive form of precocious puberty, the prevalence of breast development (for 7- to 8-year-old white girls: 5%; for 6- to 7-year-old black girls: 6.4%; and for 7- to 8-year-old black girls: 15.4%) is much closer to the likely incidence of "true precocious puberty" in young girls than what the authors propose.
- The discussion section provides additional analyses of data from the PROS study. It is important to point out the error in the authors’ calculations. They state, "only 130 girls (0.8%) [with 1 sign of puberty] would have required additional evaluation under the prevailing standards of care at the time," "only 22 girls out of the entire population of 17 077 (0.1%) ... would have met the definition of true precocious puberty under the definitions of precocity at the time," and "referral of 100%... would hardly overwhelm the current health care system, even with the current shortage of pediatric endocrinologists." Thus, the authors give the impression that "only" 0.8% of the population of all girls (as they calculated from the PROS data) would need referral. In fact, they used the wrong denominator in their calculations, a common error that occurs when cross-sectional data are treated as longitudinal data. Using the ages on which the authors are focusing, the correct denominator is the number of black girls 6 to 8 years old in the PROS study (262) plus the number of white girls 7 to 8 years old (1128), a total of 1390. Therefore, the 130 girls (55 black girls 6–8 years old and 75 white girls 7–8 years old) with a pubertal characteristic comprised 9.4% of the population of 7-year-old white girls and 6- to 8-year-old black girls, not 0.8% as stated by the authors.
- Looking at the authors’ proposal that "all girls with any secondary sexual development before 8 years of age deserve at the minimum a bone age assessment and close longitudinal follow-up," we can obtain a minimum estimate for the number of girls in the United States that would require referral for pubic hair only (we do this because a finding of pubic hair is more objective than a finding of breast tissue, which can be confused with fat tissue by a less-experienced physician). Using population estimates by race and age from the 2000 census and data from the PROS study, we can calculate an estimate for the total number of girls in the United States that would require evaluation for pubic hair alone.1,31 Applying the percentage of African American girls 3 to 8 years old in the PROS study with pubic hair to all African American girls for each year of age, we obtain 111 000 girls from 3 through 7 years of age; using the percentages of white girls in the PROS study for other US girls, we obtain 84 400 girls. This totals 195 400 girls <8 years old with at least Tanner 2 pubic hair. There are 650 pediatric endocrinologists in the United States. If all these girls truly need an evaluation, then each endocrinologist would have to see, on average, 300 of these girls. If we estimate the cost for a basic evaluation as proposed by the authors of an examination and bone age films (including radiologist interpretation) at $250, the cost to evaluate these girls would be $48 850 000. On the other hand, if the revised guidelines based on the PROS data were followed (black girls <6 years old and white girls <7 years old),2 the number of girls needing an evaluation for pubic hair drops to 63 000, a still-large but more manageable number.
We do not take issue with the fact that some girls with pubertal signs between 6 and 8 years of age will have other endocrine pathology, although acanthosis nigricans may be seen in very obese children at any age unrelated to the presence or absence of signs of puberty. No doubt, some children >8 years old have endocrine problems such as the ones found in the Midyett et al study, and they may not be identified at that age because they have fallen out of the recommended age for evaluation for many years. No system of screening is perfect. Primary care physicians should not blindly use the age of a child as a rote guide for referral. A careful history, examination, and follow-up looking for evidence of rapid progression of pubertal changes and growth acceleration should always be used in conjunction with age guidelines.
 |
CONCLUSIONS |
|---|
 TOP CONCLUSIONS SUMMARYREFERENCES |
|---|
The age of pubertal events is important individually, socially, culturally, and as a public health indicator. The rise and fall of the age of onset of secondary sexual characteristics, the attainment of gonadal maturation, and the age of complete sexual maturity may serve as the "canary in the mine" for environmental problems just as height and weight indices already do in individual cultures and countries. Growth data have been shown to be sensitive to times of stress, war, and famine, to cultural changes affecting diet and lifestyle, and to times of prosperity. In the same way, given the remarkable changes over the last few decades in the environment with regard to factors suspected of affecting puberty such as endocrine disrupters7,8,15,17 and the epidemic of overweight and obesity,3,11,14,23,27,28 pubertal events may be a sensitive indicator of conditions that are not healthful. We need to pay attention to these markers, and therefore, we find the recent pubertal studies and emerging questions and issues gratifying, especially as they relate to the quality and accuracy of pubertal measurements and clinical practice.
It is important to recognize that there are differences in the pubertal markers "age of onset of secondary sexual characteristics" and "age of menarche." The timing of these events may be regulated differently, making it important to study both. Some data have indicated that the earlier girls begin the onset of secondary sexual characteristics, the longer the time period until menarche is reached.32–34 Related to that, it is interesting to note that, in the recent study of pubertal characteristics in children with cerebral palsy by Worley et al,21 white girls began puberty earlier than the general population (25% of girls had Tanner stage 2 or greater breast development by 8.1 year of age) but did not reach menarche until later than average, at 14.0 years.
We feel it is inaccurate to posit that "girls are not gaining reproductive potential earlier than in the past,"25 given the US studies suggesting otherwise.1,2,3,22,28 The cost of evaluations alone indicates the need for additional examination of guidelines for referral for early onset of puberty in boys and girls, how factors in our environment may be affecting pubertal development, and additional studies, especially on boys, to delineate the age at which pubertal markers are occurring.
|
SUMMARY |
|---|
|
TOPCONCLUSIONSSUMMARYREFERENCES |
|---|
- Data show that girls are maturing earlier than they did several decades ago and that there are substantial racial differences between white and black girls.
- These "norms" are not the same as the condition of being "normal" in the sense of indicating optimal health. The association between earlier onset of puberty and being overweight is a clear example of this.
- Despite the fact that the PROS study population was a convenience sample, there is considerable agreement between its findings and those from the NHANES on girls.
- Consensus needs to be reached regarding the most accurate methods to assess the onset of puberty, in particular, whether breast palpation and testicular measurement is required.
- The Centers for Disease Control and Prevention need to reinstitute the collection of pubertal data in their ongoing NHANES activities after a consensus has been reached regarding accurate methodology. The age for collecting pubertal data on boys and girls should be lowered.
- Studies examining the relationship of obesity, diet, and exposure to environmental chemicals to the age of onset of puberty should continue.
- Guidelines for which children with signs of early pubertal development should be referred should be modified as new population-based data become available.
|
FOOTNOTES |
|---|
Received for publication May 5, 2003; Accepted Sep 15, 2003.
Reprint requests to (M.E.H.-G.) North Carolina Child Advocacy Institute, 311 E Edenton St, Raleigh, NC 27601. E-mail: mherman-giddens{at}unc.edu
Dr Kaplowitz’s present address: Department of Endocrinology, Children’s National Medical Center, Washington, DC
|
REFERENCES |
|---|
|
TOPCONCLUSIONSSUMMARYREFERENCES |
|---|
- Herman-Giddens ME, Slora EJ, Wasserman RC, et al. Secondary sexual characteristics and menses in young girls seen in office practice: a study from the Pediatric Research in Office Settings network.
Pediatrics.1997; 99
:505
–512
[Abstract/Free Full Text] - Kaplowitz PB, Oberfield SE. Reexamination of the age limit for defining when puberty is precocious in girls in the United States: implications for evaluation and treatment. Drug and Therapeutics and Executive Committees of the Lawson Wilkins Pediatric Endocrine Society.
Pediatrics.1999; 104
:936
–941
[Abstract/Free Full Text] - Wattigney WA, Srinivasan SR, Chen W, Greenlund KJ, Berenson GS. Secular trend on earlier onset of menarche with increasing obesity in black and white girls: the Bogalusa Heart Study. Ethn Dis.1999; 9 :181 –189[Medline]
- Liu YX, Wikland KA, Karlberg J. New reference for the age at childhood of growth and secular trend in the timing of puberty in Swedish. Acta Paediatr.2000; 89 :637 –643[CrossRef][Web of Science][Medline]
- Berkey CS, Gardner JD, Frazier AL, Colditz GA. Relation of childhood diet and body size to menarche and adolescent growth in girls.
Am J Epidemiol.2000; 152
:446
–452
[Abstract/Free Full Text] - Chang S-H, Tzeng S-J, Cheng J-Y, Chic W-C. Height and weight change across menarche of schoolgirls with early menarche.
Arch Pediatr Adolesc Med.2000; 154
:880
–884
[Abstract/Free Full Text] - Blanck HM, Marcus M, Tolbert PE, et al. Age at menarche and Tanner stage in girls exposed in utero and postnatally to polybrominated biphenyl. Epidemiology.2000; 11 :641 –647[CrossRef][Web of Science][Medline]
- Colon I, Caro D, Bourdony CJ, Rosario O. Identification of phthalate esters in the serum of young Puerto Rican girls with premature breast development. Environ Health Perspect.2000; 108 :895 –900[Medline]
- Herman-Giddens ME, Wang L, Koch G. Secondary sexual characteristics in boys: estimates from the National Health and Nutrition Examination Survey III, 1988–1994.
Arch Pediatr Adolesc Med.2001; 155
:1022
–1028
[Abstract/Free Full Text] - Reiter EO, Lee PA. Have the onset and tempo of puberty changed?
Arch Pediatr Adolesc Med.2001; 155
:988
–989
[Free Full Text] - Adair L, Gordon-Larsen P. Maturational timing and overweight prevalence in US adolescent girls. Am J Public Health.2001; 91 :642 –644[Abstract]
- Biro FM, McMahon RP, Striegel-Moore R, et al. Impact of timing of pubertal maturation on growth in black and white female adolescents: the National Heart, Lung, and Blood Institute Growth and Health Study. J Pediatr.2001; 138 :636 –643[CrossRef][Web of Science][Medline]
- Mul D, Fredriks AM, van Buuren S, Oostduk W, Verloove-Vanhorick SP, Wit JM. Pubertal development in The Netherlands 1965–1997. Pediatr Res.2001; 50 :479 –486[Web of Science][Medline]
- Kaplowitz PB, Slora EJ, Wasserman RC, Herman-Giddens ME. Earlier onset of puberty in girls: relation to increased body mass index and race.
Pediatrics.2001; 108
:347
–353
[Abstract/Free Full Text] - Krstevska-Konstantinova M, Charlier C, Craen M, et al. Sexual precocity after immigration from developing countries to Belgium: evidence of previous exposure to organochlorine pesticides.
Hum Reprod.2001; 16
:1020
–1026
[Abstract/Free Full Text] - Mul D, Oostdijk W, Drop SLS. Early puberty in adopted children. Horm Res.2002; 57 :1 –9
- Hond ED, Roels HA, Hoppenbrouwers K, et al. Sexual maturation in relation to polychlorinated aromatic hydrocarbons: Sharpe and Skakkebaek’s hypothesis revisited. Environ Health Perspect.2002; 110 :771 –776[Web of Science][Medline]
- Marshall WA, Tanner JM. Variations in the pattern of pubertal changes associated with adolescence in girls. Arch Dis Child.1969; 44 :291 –303
- Bonat S, Pathomvanich A, Keil MF, Field AE, Yanovski JA. Self-assessment of pubertal stage in overweight children.
Pediatrics.2002; 110
:743
–747
[Abstract/Free Full Text] - Wu T, Mendola P, Buck G. Ethnic differences in the presence of secondary sex characteristics and menarche among US girls: the Third National Health and Nutrition Examination Survey, 1988–1994.
Pediatrics.2002; 110
:752
–757
[Abstract/Free Full Text] - Worley G, Houlihan CM, Herman-Giddens ME, et al. Secondary sexual characteristics in children with cerebral palsy and moderate to severe motor impairment: a cross-sectional survey.
Pediatrics.2002; 110
:897
–902
[Abstract/Free Full Text] - Freedman DS, Khan LK, Serdula MK, Dietz WH, Srinivasan SR, Berenson GS. Relation of age at menarche to race, time period, and anthropometric dimensions: the Bogalusa Heart Study. Pediatrics.2002; 110(4) . Available at: www.pediatrics.org/cgi/content/full/110/4/e43
- Wang Y. Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls.
Pediatrics.2002; 110
:903
–910
[Abstract/Free Full Text] - Sun SS, Shumei S, Schubert CM, et al. National estimates of the timing of sexual maturation and racial differences among US children.
Pediatrics.2002; 110
:911
–919
[Abstract/Free Full Text] - Chumlea WC, Schubert CM, Roche AF, et al. Age at menarche and racial comparisons in US girls.
Pediatrics.2003; 111
:110
–113
[Abstract/Free Full Text] - Midyett LK, Moore WV, Jacobson JD. Are pubertal changes in girls before age 8 benign?
Pediatrics.2003; 111
:47
–51
[Abstract/Free Full Text] - Davison KK, Susman EJ, Birch LL. Percent body fat at age 5 predicts earlier pubertal development among girls at age 9.
Pediatrics.2003; 111
:815
–821
[Abstract/Free Full Text] - Anderson SE, Dallal GE, Must A. Relative weight and race influence average age at menarche: results from two nationally representative surveys of US girls studied 25 years apart.
Pediatrics.2003; 111
:844
–850
[Abstract/Free Full Text] - MacMahon B. Age at Menarche, United States. Series 11. Report No. 133NCHS. DHEW Pub. No. (HRA) 74-1615. Washington, DC: National Center for Health Statistics, Vital and Health Statistics; 1973
- Sklar C, Kaplan S, Grumbach MM. Evidence for dissociation between adrenarche and gonadarche.
J Clin Endocrinol Metab.1980; 51
:548
–562
[Abstract/Free Full Text] - US Census 2000. Available at: www.census.gov/main/www/cen2000.html. Accessed April 1, 2003
- Hagg U, Taranger J. Pubertal growth and maturity pattern in early and late maturers. Swed Dent J.1992; 16 :199 –202[Web of Science][Medline]
- Marti-Heeneberg C, Vizmanos B. The duration of puberty in girls is related to the timing of its onset. J Pediatr.1997; 131 :618 –621[CrossRef][Web of Science][Medline]
- Huen KF, Leung SS, Lau JT, Cheung AY, Leung NK, Chiu MC. Secular trend in the sexual maturity of Southern Chinese girls. Acta Paediatr.1997; 86 :1121 –1124[Web of Science][Medline]
PEDIATRICS (ISSN 1098-4275). ©2004 by the American Academy of Pediatrics
CiteULike 
Connotea 
Del.icio.us 
Digg 
Facebook 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  N. Karaolis-Danckert, A. E Buyken, A. Sonntag, and A. Kroke Birth and early life influences on the timing of puberty onset: results from the DONALD (DOrtmund Nutritional and Anthropometric Longitudinally Designed) Study Am. J. Clinical Nutrition, December 1, 2009; 90(6): 1559 - 1565. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. Cromer and C. M. Gordon Early Pubertal Development in Chinese Girls Pediatrics, August 1, 2009; 124(2): 799 - 801. [Full Text] [PDF]
|
|
|
|
 |
|
 B. Bordini, E. Littlejohn, and R. L. Rosenfield Blunted Sleep-Related Luteinizing Hormone Rise in Healthy Premenarcheal Pubertal Girls with Elevated Body Mass Index J. Clin. Endocrinol. Metab., April 1, 2009; 94(4): 1168 - 1175. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A M Bau, A Ernert, L Schenk, S Wiegand, P Martus, A Gruters, and H Krude Is there a further acceleration in the age at onset of menarche? A cross-sectional study in 1840 school children focusing on age and bodyweight at the onset of menarche Eur. J. Endocrinol., January 1, 2009; 160(1): 107 - 113. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. L. Rosenfield, R. B. Lipton, and M. L. Drum Thelarche, Pubarche, and Menarche Attainment in Children With Normal and Elevated Body Mass Index Pediatrics, January 1, 2009; 123(1): 84 - 88. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J.-C. Carel and J. Leger Precocious Puberty N. Engl. J. Med., May 29, 2008; 358(22): 2366 - 2377. [Full Text] [PDF]
|
|
|
|
 |
|
 L. S. Nield, N. Cakan, and D. Kamat A Practical Approach to Precocious Puberty Clinical Pediatrics, May 1, 2007; 46(4): 299 - 306. [PDF]
|
|
|
|
|
|
L. Ibanez, R. Jimenez, and F. de Zegher Early Puberty-Menarche After Precocious Pubarche: Relation to Prenatal Growth Pediatrics, January 1, 2006; 117(1): 117 - 121. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Deardorff, N. A. Gonzales, F. S. Christopher, M. W. Roosa, and R. E. Millsap Early Puberty and Adolescent Pregnancy: The Influence of Alcohol Use Pediatrics, December 1, 2005; 116(6): 1451 - 1456. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Denham, L. M. Schell, G. Deane, M. V. Gallo, J. Ravenscroft, A. P. DeCaprio, and and the Akwesasne Task Force on the Environment Relationship of Lead, Mercury, Mirex, Dichlorodiphenyldichloroethylene, Hexachlorobenzene, and Polychlorinated Biphenyls to Timing of Menarche Among Akwesasne Mohawk Girls Pediatrics, February 1, 2005; 115(2): e127 - e134. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. D. Jacobson, L. K. Midyett, and W. V. Moore Navigating Recent Articles on Girls' Puberty: Where Should Our Patients Go for Evaluation? Pediatrics, January 1, 2005; 115(1): 194 - 195. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
