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Secondary Sexual Characteristics in Boys
Estimates From the National Health and Nutrition Examination Survey III, 1988-1994
Marcia E. Herman-Giddens, PA, MPH, DrPH;
Lily Wang, MS;
Gary Koch, PhD
Arch Pediatr Adolesc Med. 2001;155:1022-1028.
ABSTRACT
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Background Descriptive data on pubertal stages for a representative population
of racially and ethnically diverse boys in the United States have not been
published to our knowledge.
Objective To determine at what ages boys in the United States reach each of the
5 sexual maturity stages for genital and pubic hair growth.
Design and Setting Cross-sectional survey from the National Health and Nutrition Examination
Survey III (NHANES III), 1988-1994.
Participants A population-based sample of 2114 boys aged 8 to 19 years representing
16 575 753 boys according to NHANES III sampling strategies. The
sample included white, African American, and Mexican American boys.
Main Outcome Measures Sexual maturity stages for genital maturation and pubic hair growth.
Results The median (equivalent mean) ages at stage 2 for pubic hair development
of white, African American, and Mexican American boys were 12.0 (95% confidence
interval [CI], 11.7-12.3), 11.2 (95% CI, 10.9-11.4), and 12.3 (95% CI, 12.1-12.6)
years, respectively, and at stage 2 for genital growth were 10.1 (95% CI,
9.6-10.6), 9.5 (95% CI, 8.9-10.0), and 10.4 (95% CI, 9.6-11.1) years, respectively.
All 3 groups were significantly taller and heavier than boys in previous NHANES
reports and showed earlier genital maturation and pubic hair growth than previous
studies based on Tanner staging. Statistically significant differences among
the 3 racial/ethnic groups were found in the median ages of onset of pubic
hair growth and genital development at stage 5 with and without controlling
for height and weight, indicating an earlier age of attainment for the African
American boys.
Conclusions The median (mean) ages at the onset of genital and pubic hair growth
were younger than in past studies. Additional studies are required to further
evaluate these findings and to explore the public health implications.
INTRODUCTION
DESCRIPTIVE data on the pubertal development stages of racially and
ethnically diverse boys selected to be representative of the US population
have not been published to our knowledge. In 1997, a study on girls found
significant differences in the age of onset of pubertal characteristics by
race and also found that the mean age of onset was younger compared with findings
from the last 30 to 40 years.1 Specifically,
white girls were found to begin puberty 6 months to 1 year earlier than girls
in past studies, and African American girls were found to begin puberty approximately
1 to 1.5 years earlier than white girls and to begin menses approximately
8.5 months earlier. Numerous studies worldwide have shown that the onset of
pubertal characteristics varies with race and ethnicity, environmental conditions,
geographical location, and nutrition1, 2;
thus, current geographically representative data on boys in the United States
are needed. The findings of earlier studies regarding racial differences in
pubertal timing between African American and white boys are conflicting.3, 4 To our knowledge, the only study assessing
the development of Mexican American boys, the NHANES II study of boys aged
10 to 17 years, concluded that pubertal events in this population occurred
a few months later than in white boys, but noted that comparable data were
lacking.5
Previous US studies do not provide descriptive data that are generalizable
to the entire population owing to the times of the studies,6
small sample sizes,6, 7 racial
limitations,5, 6, 7
differences in methods,4 and older ages at
entry into the studies.4, 5, 6, 7
Clinicians have relied largely on Marshall and Tanner's classic study on the
variations of pubertal changes in boys8 despite
previously described problems with such use.5, 9, 10, 11
Therefore, we undertook analysis of this cross-sectional pubertal data from
the NHANES III survey to report its findings regarding the prevalence of secondary
sexual characteristics in white, African American, and Mexican American boys
aged 8 through 19 years, and to determine if the data offer clinically useful
information.
METHODS
STUDY DESIGN AND SAMPLE
The Centers for Disease Control and Prevention (Atlanta, Ga), through
the National Center for Health Statistics (Hyattsville, Md), conducted NHANES
III to collect data during two 3-year phases from 1988 through 1991 and 1991
through 1994. This cross-sectional survey had a stratified, multistage probability
design. Although the survey was conducted in 2 phases, it was designed so
that the total sample was representative of boys in the United States. Non-Hispanic
African American and Mexican American boys were oversampled to ensure reliable
weighted population estimates for these racial/ethnic minorities. The sample
of 2495 boys aged 8 through 19 years represented 20 674 622 boys
through the respective sampling weights. This survey did not collect data
on gynecomastia, voice change, undescended testes, or facial hair growth.
The NHANES III design and methodology has been described in detail previously.12, 13
All training and assessment followed the protocol detailed below, used
in previous NHANES surveys from which prior pubertal studies have been published.3, 5 Interviewers, many of whom were Hispanic
or bilingual in Spanish and English, attended yearly training sessions to
ensure adequate and stable skills. In a similar manner, the 8 primary physicians
and the back-up physicians who examined the children were trained in conducting
sexual maturity ratings by an expert in adolescent medicine using discussion,
text, and visual aids. Sexual maturity was defined according to the 5 stages
of genital and pubic hair development, assessed by visual inspection as described
by Marshall and Tanner.8 The stages of genital
maturity were graded separately from pubic hair growth as follows:
Stage 1: The testes, scrotum, and penis are about the same size and
proportion as in early childhood.
Stage 2: The scrotum and testes enlarge and the scrotal sac reddens
and changes in texture. There is little to no enlargement of the penis.
Stage 3: There is further growth of the testes and scrotum and the penis
begins to enlarge, mainly in length.
Stage 4: The testes and scrotum continue to enlarge and the scrotal
skin continues to darken. The penis continues to grow in breadth and length
with development of the glans.
Stage 5: The genitalia are of adult size and shape. No further enlargement
takes place.
Pubic hair was staged as follows:
Stage 1: The vellus of the pubis resembles that over the abdomen.
Stage 2: Sparse growth of long, slightly pigmented, downy hair, straight
or only slightly curled, appears chiefly at the base of the penis.
Stage 3: The hair is considerably darker, courser, and more curled.
It spreads sparsely over the junction of the pubis.
Stage 4: The hair is now adult-like but the area covered is still considerably
smaller than in most adults. There is no spread to the medial surface of the
thighs.
Stage 5: The hair is adult in quantity and type, distributed in the
"male" pattern of an inverse triangle, and may spread to the medial surface
of the thighs.
Following training, the participating physicians were tested in assessing
these characteristics according to NHANES protocol, which allowed for a 1-stage
variance between the physician's assessment and the quality control standard
(e-mail communication, Kathryn Porter, MD, MS, NHANES medical officer, February
1, 2000).
The 2495 boys were examined by the participating physicians in a mobile
examination center designed for the survey. Their genitalia and pubic hair
were inspected and classified separately according to the 5 Tanner stages.
The 381 boys with missing values for any of age, race, pubic hair development
stage, or genitalia development stage were excluded; therefore, the final
sample for analysis included 2114 boys representing 16 575 753 boys
in the general population.
STATISTICAL DESIGN
All statistical analyses were conducted using SUDAAN14
(Research Triangle Institute, Research Triangle Park, NC) software for sample
surveys and accounted for the sampling weights and the primary sampling units
in the multistage probability design of the NHANES III. For descriptive purposes,
race/ethnicity by age tabulations were produced for the estimated percentages
(and corresponding 95% confidence intervals [CIs] with attainment of stage
2 or later for pubic hair and genital development. Mean heights and mean weights
were provided for additional description of each racial/ethnic group by age
(eg, age 8 years is 8.00-8.99).
We used logistic regression models to assess the relationship of age
(as a linear variable) and race/ethnicity with the presence or absence of
a particular secondary sexual characteristic. Medians (equivalent mean ages
for the underlying logistic distributions) were separately estimated for pubic
hair growth and genital development at stage 2 or later, stage 3 or later,
stage 4 or later, and stage 5 (with corresponding 95% CIs) for each ethnic
group by corresponding logistic regression models. We evaluated departures
from linearity in the relationships between presence of a characteristic and
age by adding a quadratic term to the logistic model. In cases in which the
departures from linearity were noteworthy, we used a logistic model with linear
age in a data structure that excluded either the youngest ages with 0% prevalences
and/or the oldest ages with 100% prevalences. We did not report the estimates
for median (mean) ages from those more complicated analyses since they were
similar to those from the logistic models with linear age, ie, the reported
estimates from the logistic models with linear age tended to depart from linearity.
Heights and weights from NHANES III were compared with those from the
first and second NHANES for white boys and for African American boys by a
method that controlled for age.15 For this
purpose we used subtraction to compute deviations of the height (or weight)
of each boy in NHANES III from a corresponding standardized estimate for the
same age and ethnic group from the earlier surveys; the resulting mean deviations
were compared with 0 (relative to the corresponding SEs from SUDAAN) using
an approximately normally distributed statistic. The first and second NHANES
did not provide standardized estimates for Mexican American boys and so, for
these boys, the method was modified to incorporate the standardized estimates
for white boys.
Comparisons between the ethnic groups for the percentages of boys with
development of a secondary sexual characteristic were made with logistic regression
models that simultaneously included age as both a linear variable and a categorical
variable by year (so as to account for any departures from linearity). The
influence of height and weight on these comparisons was addressed by adding
both of these explanatory variables to the logistic regression models. Also,
models that additionally included interactions of linear age with height and
weight were evaluated. Comparisons between the ethnic groups for height and
weight were made similarly with multiple linear regression models. All analyses
were carried out with PC-SAS and SUDAAN software.14, 16
RESULTS
SAMPLE
Tanner staging data were collected from 1988 to 1994 on 2114 boys of
whom 536 were white, 797 were African American, and 781 were Mexican American.
The final sample represented 16 575 753 noninstitutionalized boys
aged 8 through 19 years.
SECONDARY SEXUAL CHARACTERISTICS
Figure 1 and Figure 2 show the prevalences of pubic hair and genital development,
respectively, at Tanner stage 2 or later by age for whites, African Americans,
and Mexican Americans. Corresponding 95% CIs are presented in Table 1. At age 8 years, that is, between the eighth and ninth birthday,
no white boys had pubic hair; however, 5.3% of African American boys and 2.7%
of Mexican American boys were at least at Tanner stage 2 for pubic hair growth.
The percentages of white, African American, and Mexican American boys who
had begun genital development were 29.3%, 37.8%, and 27.3%, respectively.
At age 9 years, the proportions showing at least Tanner stage 2 pubic hair
growth were 4.3%, 21%, and 3.3% for white, African American, and Mexican American
boys, respectively and 35.7%, 58.2%, and 31.6% for genital development.
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Figure 1. Prevalence of pubic hair development
at Tanner stage 2 or later by age and race/ethnicity.
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Figure 2. Prevalence of genital development
at Tanner stage 2 or later by age and race/ethnicity.
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Table 1. Percentages of Boys With Secondary Sexual Characteristics
at Tanner Stage 2 or Later by Age and Race/Ethnicity*
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MEDIAN AGES OF ONSET OF DEVELOPMENT OF SECONDARY SEXUAL CHARACTERISTICS
Estimates of median (or equivalent mean) ages for attainment of sexual
maturity at stages 2 through 5 for pubic hair and genital development are
presented with their 95% CIs in Table 2. Pubic hair development began at a mean age of 12.0 (95% CI, 11.7-12.3)
years for white boys, 11.2 (95% CI, 10.9-11.4) years for African American
boys, and 12.3 (95% CI, 12.1-12.6) years for Mexican American boys. Genital
maturity (ie, Tanner stage 5) was reached at age 15.9 (95% CI, 15.3-16.4)
years for white boys, 14.9 (95% CI 14.4-15.5) years for African American boys,
and 15.7 (95% CI, 15.3-16.2) years for Mexican American boys. Stage 5 pubic
hair was reached at age 15.7 (95% CI, 15.3-16.0), 15.4 (95% CI, 14.9-15.9),
and 15.8 (95% CI, 15.5-16.2) years, respectively, for white, African American,
and Mexican American boys. Boys began genital development at a mean age of
10.1 (95% CI, 9.6-10.6) years if they were white, 9.5 (95% CI, 8.9-10.0) years
if African American, and 10.4 (95% CI, 9.6-11.1) years if Mexican American.
The differences in median ages for the various stages of secondary sexual
characteristics among white, African American, and Mexican American boys were
significant (P<.01) for pubic hair at Tanner stage
2 and genital development at Tanner stage 5 regardless of whether height and
weight were controlled. These differences mainly corresponded to earlier ages
of attainment for the African American boys than the white boys. Without controlling
for height and weight, Mexican American boys were significantly (P<.05) older at stages 3 and 4 for pubic hair than African American
and white boys. After controlling for height and weight, these differences
were no longer apparent.
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Table 2. Median Age of Transition to Tanner Stages 2, 3, 4, and 5 by
Race/Ethnicity*
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HEIGHTS AND WEIGHTS
Heights, weights, and population estimates by age from all 3 racial/ethnic
groups in the current NHANES analysis are shown in Table 3. These boys were significantly taller and heavier than the
boys in the previous NHANES analyses (data not shown). Within the current
NHANES sample, African American and Mexican American boys tended to be somewhat
heavier than white boys until ages 12 and 13 years when the trend reversed.
African American boys were taller than white or Mexican American boys until
age 12 years. From age 12 years on, the African American boys were shorter
than the white boys but taller than the Mexican American boys. Differences
in height (controlling for age) between whites and African Americans were
not significant; differences in height between Mexican American boys and white
and African American boys were significant (P<.001).
Comparisons between boys with stage 1 and those with stage 2 genital and/or
pubic hair development, controlling for race/ethnicity and age, were significant
for differences in height (P<.02) but not for
weight (P = .93).
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Table 3. Mean Weights, Heights, and Population Estimates for NHANES*
III Boys by Age and Race/Ethnicity
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COMMENT
According to these NHANES III data, a significant number of boys are
experiencing development of 1 or more secondary sexual characteristics, particularly
genital maturity, at very young ages. African American boys exhibited growth
of pubic hair and sexual maturity significantly earlier than white and Mexican
American boys.
The common reference for norms, Marshall and Tanner's 1969 study of
institutionalized white boys,8 found that the
mean age of onset of genital development was 11.6 years—1 years
later than the current findings. Using their mean age for the onset of pubic
hair growth (13.4 years), is not useful for our comparison because, according
to the authors, the age "was not accurately determined" because of the use
of photographs for staging. Earlier studies in the United States6, 7, 17
found that the mean age of onset for pubic hair growth ranged from age 12.2
to 12.5 years for white boys, up to a half year later than boys in this study.
Mean ages from the latter studies for onset of genital maturation were similar
to those of Marshall and Tanner.
PUBERTAL RACIAL/ETHNIC DIFFERENCES
Only a few studies in the United States have examined racial differences
in the age of onset of secondary sexual characteristics in boys. Harlan et
al,3 in their analysis of the National Health
Examination Survey Cycle III, 1966-1970, found no differences in the ages
of development between white and African American boys aged 12 to 18 years.
Biro et al4 also found no differences in the
onset of pubertal characteristics between white and African American boys
from the Cincinnati (Ohio) area who were aged 10 to 15 years at intake, although
the African American boys had slightly higher testosterone levels. A racial
difference in the onset of characteristics could have been harder to detect
because of the late ages of entry into these studies; those who developed
early would not have been recognized. Several studies of boys in the 1970s
and 1980s, assessing the relationship between sexual maturity and blood pressure
and lipid or gonadotropin levels found that African American boys were taller
and heavier and matured earlier than white boys of the same age.17, 18, 19, 20
Because 3 of these latter studies included boys as young as 5 and 6 years,
those who developed early would have been recognized.17, 18, 20
A 1994 study examining longitudinal growth data from 1974 to 1989 found that
African American boys experienced peak growth velocity earlier than white
boys, with approximately 38% having attained peak growth by age 13 years compared
with 30% of white boys.21 Recently published
data from the Bogalusa Heart Study on secular trends in the heights of children
found height increases among 9- to 12-year-old African American boys from
1973 to 1992 to be almost twice as large as those among white boys. Because
of a lack of a secular trend for increasing height among the 15- to 17-year-old
children in the study, the authors suggest that there has been an increase
in the rate of maturation rather than final height.22
(Longitudinal pubertal studies have found that boys at their peak growth velocity
are at approximately Tanner stages 3 to 4.23)
These NHANES III data indicate significant differences among white,
African American, and Mexican American boys in the age of onset of pubertal
characteristics; African American boys showed pubic hair growth approximately
9 months earlier than white boys and more than 1 year earlier than Mexican
American boys. The analysis by Villarreal et al5
of differences in pubertal onset between Mexican American and white boys based
on NHANES II data found that Mexican American boys entered puberty later than
white boys, a finding consistent with this study.
These racial/ethnic differences changed somewhat when examining the
end of puberty; ie, the attainment of Tanner stage 5. All 3 racial/ethnic
groups were within 5 months of each other between their 15th and 16th years
for pubic hair growth. However, there was a difference of 1 year between white
or Mexican American boys and African American boys in the age at completion
of genital development, with the latter being younger. When compared with
earlier studies, ages for completion of genital development and pubic hair
growth are not markedly younger,3, 5, 7, 8, 24
indicating earlier onset with a longer time to completion, a finding also
described in a recent study on pubertal development in girls in the United
States.1
We cannot explain the racial/ethnic differences. Studies have found
that African American boys have higher levels of testosterone4
and estradiol19 but whether this correlates
with earlier development is not known. The latter study19
did not find higher levels of testosterone in African American boys but did
find lower levels of androstendione. There may be racial differences in the
interactions between insulin, glucose, and androgens and hyperinsulinemia19, 25 that influence pubertal characteristics
in ways that are not clearly understood. In addition, we can speculate that
differences in diet, lifestyle, and exposure to environmental factors and
contaminants could play a role.
DATA QUALITY ISSUES
Several data quality issues need to be considered in interpreting these
data because of the degree of disparity between these results and those of
earlier studies that used Tanner ratings for sexual development. There are
several reasons to believe that these ratings are accurate. The methods used
by NHANES for training physicians in assessing sexual maturity and for collecting
and processing data have been in place for many years and are subject to quality-control
protocols as well as interrater reliability checks. A Westat (Rockville, Md)
medical consultant conducted site visits and observed the Tanner staging used
by participating physicians at least 3 times per year, comparing their ratings
with his own (e-mail communication, Brian Dolan, MD, MPH, Westat, February
1, 2000). Proportions of boys showing characteristics of sexual development
by age and race/ethnicity are consistent both in the yearly increases in the
number of boys with a given characteristic and also across racial/ethnic groups.
In addition, the boys in our survey were taller and heavier at earlier ages
than those in the past; therefore, earlier sexual development would also be
expected. Finally, there were significant differences in height for all 3
racial/ethnic groups between boys at stage 2 and boys who were not. If the
clinicians were making errors in their assessment of stage 2 puberty, we would
not expect this consistent finding. Several pubertal studies on boys have
documented genital growth in boys as young as 9 years.6, 7, 17, 19, 24, 26
It is interesting to note that 20 years ago the mean age for the attainment
of genital stage 2 for Egyptian boys from the highest social class was 10.1
years,26 while the mean age for boys from other
parts of the world has been as young as 9.1 years.2
On the other hand, Tanner staging (by observation) of male genital development,
as with female breast development, is somewhat subjective since actual measurement
or palpation techniques are not used. The changes in genital development indicating
the transition from stage 1 to stage 2 (ie, enlargement of the testes and
slight thinning and reddening of the scrotal skin) are probably harder to
detect visually than breast changes in girls. However, the earlier NHANES
studies using the same training and examination methods3, 5
reported the usually expected 6 months to a year difference between the onset
of genital and pubic hair growth. In addition, according to NHANES personnel,
the genital examination was sometimes uncomfortable both for the physicians
and the subjects since the boys, dressed in paper gowns and underwear, had
to remove their underwear for the Tanner staging (e-mail communication, Brian
Dolan, MD, MPH, February 1, 2000). Although it has been noted that staging
of genital development by visual inspection alone (Tanner staging) may be
an unreliable determination of gonadal growth,4, 24
many well-known studies on puberty are based on this method, including Marshall
and Tanner's 1970 study, which is commonly used for clinical norms.3, 5
These data have other limitations. While statistical methods allow the
calculation of median or mean ages of attaining various characteristics with
cross-sectional data, other aspects of pubertal growth such as duration, peak
height velocity, or examining the relationship between duration and timing
of stages can only be examined in longitudinal studies. Also, this NHANES
did not collect data on gynecomastia, a common problem for adolescent boys,
voice change, or axillary and facial hair growth. Finally, data on boys younger
than 8 years were not collected even though a sizable proportion between ages
8 and 9 years had already begun genital growth according to the findings.
There are several conclusions that may be drawn from this analysis.
First, it is clear that additional studies need to be done to either confirm
or refute these findings. Given the importance of obtaining accurate pubertal
data for medical, sociological, and psychological use, as well as assessing
environmental influences, it is unfortunate that the NHANES survey currently
being used in the field does not include collection of pubertal data and that
the inclusion of such data is not planned for the future. Given the ability
of NHANES to study a population-based sample that is generalizable to the
US population as a whole, this change in their survey design is disappointing.
Should future NHANES surveys again include sexual maturity staging, collection
of pubertal data on much younger children is needed to recognize those who
mature very early. Additionally, the examination should be performed by clinicians
with extensive experience with the pediatric population and in a setting as
comfortable and noninvasive as possible, a goal that would likely require
a complete physical examination.
Second, these data do support significant racial and ethnic differences
in sexual maturation, especially in the development of pubic hair. Third,
the data suggest that boys in the United States are experiencing the onset
of pubic hair growth earlier than in the past and may be experiencing earlier
genital development, a finding that demands further study. Finally, earlier
onset of puberty raises important clinical and public health implications,
especially regarding the effect of diet and endocrine disrupters on pubertal
development as has been indicated by a sample of articles following the outcome
of the recent study on girls.1, 27, 28, 29, 30, 31
Issues that need addressing and further study include possible revision of
sex education programs, anticipatory guidance, and clinical standards; the
need to research causes that may be related to diet, culture, lifestyle, and
environment; and understanding whether earlier puberty onset may have any
long-term effects on health.
AUTHOR INFORMATION
What This Study Adds
There are no published data on pubertal characteristics of boys in the
United States of varied racial/ethnic groups representative of the population
at large. The NHANES data collected by the federal government provide an opportunity
to examine Tanner stages for genital developmentand pubic hair growth for
whites, African Americans, and Mexican Americans.
The findings suggest that the norms from Marshall and Tanner's 1970
study may no longer be appropriate, especially for boys who are not white.
The data also suggest that onset of puberty in boys may be earlier than in
the past, that there are racial and ethnic differences, and that additional
studies are required to confirm or refute the NHANES results.
Accepted for publication May 10, 2001.
This study was supported by grant 993-C17 from Genentech Inc, South
San Francisco, Calif.
From the Departments of Maternal and Child Health (Dr Herman-Giddens)
and Biostatistics (Ms Wang and Dr Koch), School of Public Health, University
of North Carolina at Chapel Hill. Dr Herman-Giddens is also a senior fellow
at the North Carolina Child Advocacy Institute, Raleigh.
Corresponding author: Marcia E. Herman-Giddens, PA, MPH, DrPH, 1450
Russell Chapel Rd, Pittsboro, NC 27312 (e-mail: mherman-giddens{at}unc.edu).
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