Puberty and its measurement: a decade in review
JOURNAL OF RESEARCH ON ADOLESCENCE, 21(1), 180 – 195
Puberty and Its Measurement: A Decade in Review
Lorah D. Dorn and Frank M. Biro
Cincinnati Children's Hospital Medical Center and University of Cincinnati
Since the early 1980s, the focus on the importance of puberty to adolescent development has continued with variability inthe methodology selected to measure puberty. To capture the relevant and important issues regarding the measurement ofpuberty in the last decade, this paper will address (1) the neuroendocrine aspects of puberty and its components, as well asthe timing of puberty and its tempo; (2) why puberty is measured, including the relevance of puberty and its timing tohealth and development as well as the relevance of being off-time, that is, early or late with respect to a reference group; (3)the measurement of puberty and its methodology with respect to pubertal staging by physical examination, self-reportmeasures, and their agreement with other methods and measures, hormones and their methods of measurement, andcomparison of hormone concentrations to pubertal stage; and (4) recommendations for what is needed in the next decaderegarding the measurement of puberty.
Puberty was recognized as early as ancient Greek
lescents (Petersen, Tobin-Richards, & Boxer, 1983).
history. In the scientific and lay literature of the past
With her investigations came the development of the
60 years, there has been an awareness of the impact
Petersen Pubertal Development Scale (PDS; Petersen,
of puberty on multiple facets of adolescent devel-
Crockett, Richards, & Boxer, 1988), a self-report
opment. The external physical changes of puberty
measure focusing on physical changes in growth and
were evident, and individuals in the adolescent's
development that represents some of the early pub-
environment often surmised that pubertal develop-
ertal changes (e.g., breast development) but that is
ment impacted emotional and behavioral issues as
more heavily weighted toward those that become
well as adjustment in the lives of adolescents. Im-
evident in mid- to late puberty for both boys (e.g.,
portantly, however, empirical studies that objectively
facial hair, voice change) and girls (e.g., menarche).
quantified puberty were not evident until the 1940s
During a similar time frame, studies examining pu-
and 1950s, when Reynolds and Wines captured the
berty with psychosocial variables used self-report
physical changes of puberty in both girls and boys
along with line drawings of maturational stages
(Reynolds & Wines, 1948, 1951). This was followed
(Morris & Udry, 1980), whereas others conducted
by the classic works of Tanner and colleagues with
physical examinations for pubertal staging and col-
the five-level graded categories of pubertal devel-
lected blood for serum pubertal hormone concen-
opment for girls and boys (Marshall & Tanner, 1969,
trations (Brooks-Gunn & Warren, 1989; Nottelmann
1970; Tanner, 1962). ‘‘Tanner'' staging remains the
et al., 1987; Susman, Nottelmann, Inoff-Germain, &
primary system used for pubertal staging.
Dorn, 1987).
Combining the measurement of puberty with key
To capture relevant issues on the measurement of
aspects of adolescent development (e.g., socioemo-
puberty in the last decade, this paper will address
tional, cognitive, behavioral) first became evident in
four primary areas. First, puberty will be defined
the 1950s when Jones and colleagues (Jones & Bayley,
and described in terms of the neuroendocrine as-
1950; Mussen & Jones, 1957) reported on the impact
pects of puberty and its components as well as the
of timing of puberty on later development. In those
relative timing of puberty and its tempo. Second, the
reports, bone age was used as a measure of pubertal
rationale of why puberty is measured will be dis-
development. Studies then followed that examined
cussed, including the relevance of puberty and its
linear growth and age at peak height velocity as a
timing in understanding health and development as
measure of puberty. It was not until the late 1970s
well as its relevance to psychological and behavioral
that Petersen began her classic longitudinal study
development. Third, the methodology of the mea-
focusing on biopsychosocial changes in early ado-
surement of puberty will follow. Specifically, pub-ertal staging by physical examination will beincluded along with self-report measures and their
Requests for reprints should be sent to Lorah D. Dorn, Cincin-
r 2011 The Authors
nati Children's Hospital Medical Center, Division of Adolescent
Journal of Research on Adolescence r 2011 Society for Research on Adolescence
Medicine, MLC 4000, Cincinnati, OH 45229. E-mail:
PUBERTY AND ITS MEASUREMENT
agreement with other methods and measures, fol-
of kisspeptins from the KISS1 gene and its receptor, G
lowed by methods of hormone measurement and
protein-coupled receptor 54 (GPR54) or KISS1r re-
comparison of hormone concentrations to pubertal
ceptor. Kisspeptin and KISS1 are linked as regulators
stage. The paper will conclude with recommenda-
to reproduction and pubertal initiation (Banerjee &
tions for what is needed in the next decade regarding
Clayton, 2007; de Roux et al., 2003; Seminara et al.,
the measurement of puberty.
2003). In the brain, kisspeptin neurons signal andactually stimulate GnRH neurons; with respect topuberty, they are ‘‘triggering and guiding the tempo
of sexual maturation'' (Oakley, Clifton, & Steiner,2009). Additional studies have examined adolescents
Neuroendocrine Aspects of Puberty
with abnormal timing of puberty to determine a ge-
Puberty is a process, not an event, that results from
netic component to timing of onset (Gajdos, Hirsch-
a complex series of coordinated neuroendocrine
horn, & Palmert, 2009; Wehkalampi, Widen, Laine,
changes leading to internal and external physical
Palotie, & Dunkel, 2008). Further knowledge of the
changes in primary and secondary sexual charac-
triggers for onset and tempo of puberty is potentially
teristics and eventual reproductive competence. Pu-
relevant to understanding an association between
berty occurs between childhood and adulthood and
psychological development and abnormal puberty.
is initiated in the brain after reactivation of the hy-
For example, males with constitutional delay and
pothalamic – pituitary – gonadal (HPG) axis. This se-
functional hypogonadotropic hypogonadism were
quence of events has been known for decades, first
noted to have attention deficit disorder (Sedlmeyer &
observed from lower animal models. Gonadotropin-
Palmert, 2002).
releasing hormone (GnRH) neurons undergo reacti-vation from the previous fetal and neonatal periods
Components of Puberty
via the GnRH pulse generator (Grumbach & Styne,2003; Knobil, 1988; Plant, 2002). During the pre- and
There are two distinct yet overlapping components
perinatal periods of development, an increase in go-
of puberty particularly relevant to its measurement
nadal steroids is responsible for sexual differentiation
(Grumbach, 2002): adrenarche and gonadarche. Ad-
as well as organizing neural systems. In the first year
renarche, or ‘‘awakening of the adrenal glands,'' in-
of postnatal life, the GnRH pulse generator becomes
cludes maturation of the adrenal gland and the
quiescent until its reactivation before pubertal onset.
ensuing rise of adrenal androgens (e.g., dehydroepi-
As much as 1 year before the external changes of
androsterone [DHEA], its sulfate [DHEAS], and
puberty are evident, reactivation of the secretion of
androstenedione; Grumbach & Styne, 1992). This rise
GnRH occurs from the median eminence of the hy-
occurs around ages 6 through 8 years in girls and
pothalamus in a pulsatile fashion. In turn, GnRH
about 1 year later in boys (Cutler et al., 1990; Parker,
stimulates the pituitary gland to release gonadotro-
1991). These androgens continue to rise during go-
pins (luteinizing hormone [LH] and follicle-stimu-
nadarche and on into the third decade of life (Saenger
lating hormone [FSH]) into the circulation, first
& DiMartino-Nardi, 2001). Adrenal androgens are
during sleep (Ojeda et al., 2006). The amplitudes of
primarily responsible for axillary and pubic hair, but
LH and FSH pulses increase. These increases even-
such development does not occur immediately when
tually lead to production of estradiol and testosterone
adrenarche begins. Adrenal androgens must reach
from the target tissues of the ovary and testes, re-
concentrations high enough to meet the sensitivity of
spectively. With the stimulation of these gonadal
the target tissue at the hair follicles. Adrenal andro-
steroid hormones, breast and uterine tissue, as well as
gens also are considered neurosteroids (Maninger,
the testes and phallus, increase in size and structure.
Wolkowitz, Reus, Epel, & Mellon, 2009) and thus
Regulation of the HPG axis occurs through an in-
may contribute to behavior and psychological pro-
tricate feedback system that matures during puberty
cesses. Further, it is believed that onset of adrenarche
and, in healthy individuals, remains functional
is a necessary component for the subsequent occur-
throughout the reproductive years. The mechanisms
rence of gonadarche.
for reactivation of this system remain somewhat of a
Little is known about the mechanism for onset of
mystery, particularly in human adolescents. There are
adrenarche. Lack of knowledge may be due to the
likely numerous permissive signals that trigger
fact that adrenarche occurs only in higher primates,
pubertal onset, including the hormones leptin and
and thus lower animal models cannot be used
ghrelin as well as body composition (Sisk & Foster,
to study its development. Belgorosky, Baquedano,
2004). New in this decade was the exciting discovery
Guercio, and Rivarola (2009) provided a recent
review on the development of adrenarche in which
timing of puberty, particularly in girls. Ong, Ahmed,
they indicated multiple factors are likely involved,
and Dunger (2006) described how the secular trend
including both local changes in the adrenal gland as
in age at menarche has slowed or stopped in many
well as peripheral metabolic changes. In particular,
Western countries. However, they indicated that
the review summarized newer information and fo-
in subgroups with nutritional deprivation, age at
cused on the growth hormone-insulin-like growth
menarche may continue to fall even as nutrition and
factor (GH-IGF) axis and insulin sensitivity as well as
social class improve in countries as they develop. In
the estrogen receptor and GPR30 pathway. The field
U.S. studies, the majority of a panel of experts agreed
would benefit from further studies regarding ad-
that puberty was occurring earlier in girls from 1940
renarche's trigger.
to 1994 and was confirmed by Aksglaede et al.
Gonadarche, the second component of puberty,
(2009), but insufficient evidence was available to
occurs with reactivation of GnRH neurons (see the
note changes of pubertal onset in boys (Euling et al.,
Neuroendocrine Aspects of Puberty section) and se-
2008). Although the study methodologies may differ
cretion of estradiol and testosterone. In gonadarche,
(e.g., pubertal measures), this secular trend is gen-
the primary sex organs develop (ovaries, testes) and
erally accepted in girls and is now thought to be
external signs of puberty (e.g., breast and genital
relatively stable (e.g., little recent change) with re-
development) begin, leading subsequently to repro-
spect to age at menarche in European girls (Parent
ductive competence. These external signs are used in
et al., 2003). Specifically, pubertal onset in girls
the staging process of puberty as described by Tanner
occurs earlier in African Americans compared with
(Marshall & Tanner, 1969, 1970): Stage I, prepubertal;
Caucasians, and age at menarche has not fallen at the
Stage II, breast and genital development indicating
same rate as onset of puberty.
entry into puberty; and up to Stage V, full maturity.
The literature is more controversial surrounding
Pubic hair is also staged from I to V (see the Mea-
the impact of timing of puberty on height and
surement of Puberty and Its Metholodogy section).
growth parameters. Most studies agree that later
In considering the role that puberty may play in
onset of puberty is associated with lower peak height
psychological and behavioral development, both
velocity and pubertal height gain in girls (Vizmanos,
adrenarche and gonadarche may be relevant. Each
Martı´-Hennenberg, Cliville, Moreno, & Fernandez-
component represents a different endocrine axis as
Ballart, 2001). Age of pubertal onset affects the in-
well as different external physical characteristics.
tensity and duration of the pubertal growth peak but
Thus, it is important to consider the outcome vari-
not final height in girls (Biro et al., 2001; Vizmanos
able when selecting a measure of puberty that rep-
et al., 2001) and in boys (Vizmanos et al., 2001). The
resents one axis rather than the other. One should
literature is mixed regarding timing of pubertal onset
ask, does the outcome reflect the gonadal or adrenal
and adult height in traditional studies as well as in
axis? Rarely is it wise to combine the two stages by
studies published in the last decade. For example,
taking the average (e.g., breast and pubic hair).
studies have reported no impact of timing of pu-bertal onset on adult height (Vizmanos et al., 2001),whereas others noted that early maturers are shorter
Timing of Puberty
as adults (Biro et al., 2001). Two recent publications
In the previous decade, the scientific community was
were important in this decade and may shed some
stunned by a controversial publication proposing
light on these apparent disparities. Bratberg, Nilsen,
that the timing of puberty in girls occurred earlier
Holmen, and Vatten (2006) noted that early matura-
than in the past (Herman-Giddens et al., 1997). This
tion led to shorter adult stature only in those with
cross-sectional study, based on more than 17,000 girls
lower body mass index (BMI). Huang, Biro, and
in the United States, noted that puberty began as
Dorn (2009) investigated relative timing through or-
early as age 6 or 7 based on breast development, but
dinal logistic regression and found that when men-
age at menarche did not show a similar decline. The
arche was used as the basis of timing, early-maturing
controversial methodological issues of the study
girls were shorter as adults; however, when onset of
have been articulated elsewhere (Emans & Biro,
breast development was used to determine timing,
1998; Reiter & Lee, 2001; Rosenfield et al., 2000), and
there was no impact of timing on adult height. As
some subsequent publications suggest minimal
these publications demonstrate, the pubertal pa-
changes in age of onset of puberty (Sun et al., 2002).
rameters selected by investigators may impact the
However, the majority of recent studies primarily
conclusions. Although most investigators agree that
conducted in the United States and Northern and
earlier-maturing youth have a greater height velocity,
Western Europe have begun to document an earlier
BMI may interact with timing to impact final height
PUBERTY AND ITS MEASUREMENT
and may affect how investigators define timing
ature. An inverse correlation exists between the on-
(relative to which pubertal event is selected or which
set of puberty and the interval between onset of
mathematical model is used to determine onset).
puberty and menarche; that is, the tempo through
To make a cross-cultural comparison of timing of
puberty is longer with early maturers and shorter
puberty, we will focus on some of the international
with late maturers. The correlation in girls is
studies pertaining to timing of puberty published in
.28 (Biro et al., 2006) to
the last decade. Importantly, some of the studies
Hennenberg & Vizmanos, 1997). A similar associa-
were conducted in developing or transforming coun-
tion was noted by Pantsiotou et al. (2008), although
tries, whereas others represent more recent Euro-
high attrition in the longitudinal study raises con-
pean studies that likely have not been reviewed
cern about a biased sample.
elsewhere. Table 1 describes such studies for boys
Few studies have examined the impact that tempo
and girls, in which the majority shows an earlier
of puberty has on psychosocial development in ad-
pubertal onset.
olescence. How quickly (or slowly) an adolescentprogresses from one stage to another may have im-plications for his or her self-perception, perception
Pathways of Puberty
by others, or even for alterations in mood or behavior
In the vast majority of girls, thelarche (breast devel-
considering that receptors for puberty-related hor-
opment) is thought to be the first visible secondary
mones are evident in the brain. Ge et al. (2003) con-
sexual characteristic followed by the appearance of
ducted an important study on African American
pubic hair. In some cases, pubic hair may begin first
boys and girls aged 10 – 12 years in which they re-
or both breast and pubic hair may appear simulta-
ported boys with accelerated pubertal maturation
neously. In boys, increase in testicular volume is
across two times also showed the greatest increase
generally first. Although most studies focus on the-
in depressive symptoms. However, an alternate
larche as the first sign of puberty in girls, Biro and
view was reported in which boys with accelerated
colleagues report two papers in this decade on the
pubertal maturation (aged 10 – 12 and 12 – 14 years)
issue of thelarche and pubarche (pubic hair first)
had a lower risk of depression (Laitinen-Krispijn,
(Biro et al., 2006; Biro, Huang, Daniels, & Lucky,
van der Ende, & Verhulst, 1999). Based on these
2008). In the longitudinal National Growth and
disparities, it is important to further examine the
Health Study, Biro et al. (2003) examined two groups
impact of tempo on psychosocial development in the
of White girls who had asynchronous development;
next decade.
that is, either thelarche or pubarche occurred first butnot both simultaneously. They reported age of onsetof maturation in the two groups was similar, but the
WHY MEASURE PUBERTY?
thelarche group had greater adiposity and pon-
Relevance of Puberty and Timing of Puberty to
derosity at pubertal onset as well as throughout
Health and Development
puberty. In a subsequent report of 9-year-old Blackgirls and White girls (n 5 478) from the same data
The importance of puberty and timing of puberty to
set, the authors argued that height velocities of the
adolescent health and development is not always
pubarche and thelarche groups did not differ and
recognized. Numerous studies examining biological
that both were in the pubertal range. Thus, both
phenomena or physical health outcomes have ne-
pathways may represent onset of puberty (Biro et al.,
glected to measure puberty and account for its con-
2008). Other investigators have examined the impact
tribution; thus, potentially erroneous conclusions in
of pathway, confirming the relationship (Christensen
outcomes can be made. Several decades ago, Hein
et al., 2010; Schubert et al., 2005). It would be desir-
(1987) addressed the impact that puberty may have
able for the National Children's Study to examine
on metabolic and therapeutic effects of pharmaco-
this issue with research-grade physical examinations
logic agents. She subsequently demonstrated how
because the study will be longitudinal and in a more
Tanner stage was associated with the half-life of an
recent cohort of both boys and girls.
asthma medication and that chronological age alonewas not the best way to determine dosage duringpuberty when rapid growth is occurring (Cary, Hein,
& Dell, 1991). Still, only a few noteworthy studies are
Tempo of puberty (progression to established mile-
including pubertal stage by physical examination
stones after entry into puberty) is an understudied
when testing a physiological hypothesis. With rare
phenomenon in the psychosocial and medical liter-
exception (see Feinberg, Higgins, Khaw, & Campbell,
PUBERTY AND ITS MEASUREMENT
2006), the norm tends either toward neglecting
Kaplowitz & Oberfield, 1999), PA is still defined in
measuring puberty or toward measurement by
the literature as occurring in girls 8 years of age or
self-report. Understanding how the physiology of
younger and in boys aged 9 years or younger (Siegel,
puberty may impact physical or mental health con-
Finegold, Urban, McVie, & Lee, 1992). PA is more
ditions, treatment regimens, or behaviors would
common in girls than in boys. In PA, adrenal andro-
enhance knowledge and improve outcomes.
gens are found in higher concentrations than in
In the psychosocial literature, puberty or timing of
on-time adrenarche peers and, thus, pubic hair is
puberty has often been recognized as an important
evident. Additionally, body odor and acne may also
factor in various outcomes. Overall, earlier timing of
be apparent as well as increased linear growth. It is
puberty has been shown to be associated with or be a
generally believed that gonadarche and menarche do
risk factor for negative psychological (e.g., depres-
not present any earlier in girls with PA; notably, there
sion) and behavioral (e.g., risky behaviors, acting
may be some discrepancy in that contention.
out) outcomes, but there are exceptions. Puberty may
PA is referred to as benign when no pathological
be an important factor because it may impact the
source is determined (e.g., no pituitary or adrenal
phenomenon under study either directly (e.g., brain
tumor). Although PA is usually considered benign,
changes occur at different times during puberty and
an expanding body of literature suggests otherwise
in turn may impact neuropsychological function or
(Iba´n˜ez, DiMartino-Nardi, Potau, & Saenger, 2000).
behavioral changes) or indirectly (e.g., parents or
In brief, girls with PA are at higher risk for
peers notice external pubertal changes in an adoles-
developing disorders in adulthood, including poly-
cent and in turn respond differently to the adoles-
cystic ovarian syndrome (PCOS) and/or metabolic
cent). Alternatively, it may be that underlying
syndrome, with a complex of other health issues and
concentrations of sex hormones are influencing out-
complications associated with both. More recently,
comes. Maturation can be studied directly through
girls with PA have been described as experiencing
hormone concentrations or indirectly through puber-
more mood disturbances and behavioral problems
tal staging as the hormones influence the degree of
(Dorn, Hitt, & Rotenstein, 1999; Dorn et al., 2008),
physical development. Thus, in all these cases, it is
indicating that the disorder may have ramifications
important to measure puberty accurately so as to
beyond physical health.
understand whether puberty is contributing to the
PP refers to early gonadarche, occurring as young as
outcome under study. Many psychosocial studies
toddlerhood to age 6 years. As in PA, PP occurs more
have used self-report of pubertal status or timing,
commonly in girls than in boys and can be the result
which sometimes has been appropriate. However,
of a tumor. However, the etiology of PP is often un-
some psychosocial outcomes may have an underly-
known, especially in girls. PP can be treated phar-
ing biological component (e.g., depression). We have
macologically with agents that temporarily ‘‘turn off''
argued for the necessity of selecting a measure of
the HPG axis. These medications include leuprolide
puberty that is congruent with the outcome under
acetate, given as an injection every 1 or 3 months, and
study (Dorn, Dahl, Woodward, & Biro, 2006). Un-
histrelin acetate, a newer, long-acting implantable
fortunately, many select the measure that is easier to
delivery system. Pharmacotherapy is stopped once
collect rather than the measure that is more appro-
bone age is concordant with chronological age and
priate to the scientific and theoretical aspect of the
adult height prediction is significantly improved. If left
study. In the following paragraphs, we provide ex-
untreated, children with PP are unlikely to reach their
amples of studies examining the relevance of ‘‘clin-
full height potential as adults. Psychological concerns
ically early'' onset of puberty along with those
also surface at the onset of PP and may continue into
investigating the relevance of early puberty with
adolescence. Recent studies show that girls with PP
respect to peers when examining physical as well as
have internalizing problems and poor self-image
(Baumann et al., 2001; Officioso et al., 2000); see arecent review by Dorn (2007).
Relevance of puberty that is clinically early. Two
There is a lack of recent studies of PP and PA
clinical examples that represent more extreme cases
that examine psychosocial or cognitive issues. More
of early puberty are found in children manifesting
in-depth studies with PP and PA children using bio-
either premature adrenarche (PA) or precocious
behavioral methodologies could enhance our under-
puberty (PP). Although puberty is described in the
standing of normal puberty. Off-time PP and PA children
most recent literature as occurring earlier than in
may experiences parallel changes as do youth
past decades (e.g., breast development before age 6
who are older and experience on-time and normal
in Black girls and before age 7 in White girls;
Relevance to Physical Health of Clinically Early
the life history theory focusing on timing of puberty
Puberty That Is Not ‘‘Abnormal''
and the structure and processes in families (Ellis &Essex, 2007). For a review of family influences, see
Puberty has a tremendous impact on health and
Susman and Dorn (2009).
well-being (Patton & Viner, 2007). Previous studieshave noted that early onset of menarche is associatedwith risk of breast cancer; however, this association
MEASUREMENT OF PUBERTY AND ITS
is weakened considerably when age at peak growth
is included in the analysis. Menarche may serve as aproxy for age at peak growth, or both factors may
reflect age at onset of puberty (Kindblom et al., 2006).
In the last decade, no new measures of puberty have
Similarly, women who reached maximum height at a
emerged. Importantly, two reviews pertinent to
young age (under 12 years) had a much greater risk
measuring puberty appeared. First, Coleman and
of breast cancer (Li, Littman, & White, 2007). Of note,
Coleman (2002) provided a review on the measure-
younger age at peak growth is associated with
ment of puberty. This was followed by a later paper
greater growth velocity, as stated earlier. Addition-
that emphasized the necessity of measuring puberty,
ally, tall as well as obese children have greater levels
reviewed measures of pubertal status and timing,
of IGF-1 in response to growth hormone, which may
and characterized potential ways of determining the
account for the increased risk of some cancers later in
appropriate measure of puberty for a research study
life (Bouhours-Nouet, Gatelais, Boux de Casson,
(Dorn et al., 2006). In the following paragraphs, we
Rouleau, & Coutant, 2007). Few studies report on the
update the status of some of the issues pertaining to
impact that puberty may express in physical health
measuring puberty that have emerged or persisted in
in males. An excellent review of the issues sur-
the last decade.
rounding pubertal timing and physical health is
Dorn et al. (2006) addressed several issues that
available (Golub et al., 2007). Most of these studies
emerged in the literature regarding the actual mea-
use age at menarche and look at outcomes quite
surement of puberty. First, the gold standard for
distal to puberty. Few look at the impact of puberty
measuring pubertal status continues to be physical
on more proximal health issues.
examination by a trained clinician using the criteriaattributed to Tanner (Marshall & Tanner, 1969, 1970),including staging of breast and pubic hair for girls
Relevance to Psychosocial Development of Early
and genital and pubic hair for boys. With respect to
Puberty Not Clinically ‘‘Abnormal''
breast development, staging was originally done by
Extensive literature can be found regarding the im-
visualization (Marshall & Tanner, 1970). The current
pact of timing of puberty on psychosocial develop-
consensus is that staging is best done by palpation
ment. The majority of these studies continue to use a
and visualization so one can distinguish breast tissue
self-report measure of puberty regardless of the fo-
from adipose tissue; as rates of obesity continue to
cus of the study. With rare exception (see Ellis &
rise, it becomes relevant to distinguish adipose tissue
Essex, 2007), most literature focuses on timing of
from breast tissue. In our review of the literature and
gonadarche rather than adrenarche. In the literature
in numerous discussions with investigators, contin-
on girls, findings generally show that early timing of
ued reluctance lingers for measuring puberty by
puberty is a risk for various affective states and
physical examination in situations that would rec-
negative behaviors (Mendle, Turkheimer, & Emery,
ommend doing so. Numerous investigators state that
2007; Susman & Rogol, 2004). Over the past decade,
parents and adolescents are not likely to consent to a
such studies have continued their trend of more
physical examination or that other obstacles impede
studies conducted in girls than boys, with few lon-
conducting them. This unfortunate lack of staging by
gitudinal studies evident (for exception, see studies
physical examination hampers advancement in our
by Angold and Costello [e.g., Costello, Sung,
understanding of puberty and its impact on many
Worthman, & Angold, 2007]). We refer the reader to
outcomes. Second, we and others have identified
several excellent sources for reviews on the timing of
limitations in the photographs of breast, genital, and
puberty and its impact on psychosocial development
pubic hair used for pubertal staging. The Tanner
(Angold & Costello, 2006; Negriff & Susman, in
photographs were taken decades ago and include
press; Reardon, Leen-Feldner, & Hayward, 2009).
only White youth. Although higher-quality photo-
This past decade also brought with it more evidence
graphs are available (van Wieringen, Roede, & Wit,
on family influences of timing of puberty, including
1985), to our knowledge, no studies are using them
PUBERTY AND ITS MEASUREMENT
in their research. Further, no photographs are avail-
stage. In the first study, reliability of the PDS was
able for pubertal stages of other races/ethnicities,
examined in a group of 10- to 18-year-old male and fe-
limiting the examination of potential differences in
male Black, multiethnic South African youth (Norris &
characteristics. A third issue involves the method-
Richter, 2008). The investigators reported that the PDS
ological problems of measuring puberty that could
was less reliable than physical examinations. Further,
enhance the reliability and reproducibility of studies.
when comparing the PDS to sexual maturity ratings by
Frequently, methods sections contain scant informa-
examination, k coefficients were very low in females
tion about training/certification and interrater
and percent agreement was 26% in males. The
agreement for physical examination or other infor-
investigators indicated that the features measured in
mation relevant to determining staging quality.
the PDS may not always be relevant to this population
When studies have used self-report, the specific
or that progression of these indicators may vary in this
methodology may also be missing, thus making it
population (Norris & Richter, 2008). To our knowledge,
difficult to ascertain the quality of the article. By
this is the first international study involving Black,
addressing all of these issues, the quality of pubertal
multiethnic youth that examined agreement between
research could be enhanced.
physical exams and the PDS. Based on the study,investigators should be cautious in using the PDSwithout further testing in similar samples. The
Self-Report Measures
second international study examined agreement of
Self-report continues to be a popular way to account
physical examination with self-report in 354 Chinese
for pubertal development in research studies,
children using line drawings and a brief explanation
including reports by the adolescent using either
(Chan et al., 2008). k coefficients were generally strong
photographs (Dorn, Susman, Nottelmann, Inoff-
(.72 and .83 in girls and .58 and .80 in boys,
Germain, & Chrousos, 1990) or line drawings (Mor-
respectively). The third study included a small
ris & Udry, 1980) of pubertal stages or using the PDS
sample of 47 male and female elite Canadian athletes
(Petersen et al., 1988), the most widely used measure
who were 12 – 17 years of age (Leone & Comtois, 2007).
of self-report over the years. Few studies in this de-
Comparing physical examination to self-report by line
cade have examined interrater agreement of self-
drawings, k coefficients were high for both boys
report of puberty and assessment by physical
(k 5 .79, genital; .67, pubic hair) and girls (k 5 .85,
examination by trained health care providers. In the
breast; .75, pubic hair). Agreement may have been
paragraphs that follow, we review such studies but
influenced by the small size per cell and by the
also cite studies that compare two types of self-report
restricted range owing to large percentages in Stages
measures. Although the latter seems less relevant
without a comparison with the gold standard of a
Three studies included adolescents with varied
physical examination, self-report does provide an
anthropomorphic characteristics. First, Bonat, Path-
estimate of maturation that often is biased.
omvanich, Keil, Field, and Yanovski (2002) includedoverweight girls and boys aged 6 – 12 years. Of the 244
Agreement of self-report and physical exam-
participants, 41% were defined as obese. Kendall rank
Wu, Schreiber, Klementowicz, Biro, and
correlations with physical examination and self-report
Wright (2001) examined agreement of self-assessment
for breast stage were .37 in obese and .54 in nonobese
of puberty (areolar and pubic hair) via line drawings
girls and for pubic hair were .64 in obese and .66 in
with examiner assessments in 1,396 healthy girls aged
nonobese girls. Boys' pubic hair stage had a correlation
11 – 14 years. k coefficients were relatively low and
of .45 in obese and .35 in nonobese participants. The
ranged from .32 to .55. In a second study of healthy
authors concluded that self-report was not very
accurate for breast development, particularly in obese
Lipaczewski, and Haynatzki (2006) reported that k
girls, and for pubic hair development in both groups of
coefficients were moderate for girls' ratings of breast
boys (Bonat et al., 2002). The second study included
and pubic hair (k 5 .49 and .68, respectively) and boys'
100 children with Crohn's disease (aged 8 – 18 years). k
ratings of pubic hair (k 5 .49). Genital staging was not
coefficients were high (.74 – .85) when comparing
reported in boys. Desmangles and colleagues suggest
physician ratings to self-report by line drawings
that self-report was not reliable and, therefore, not
(Schall, Semeao, Stallings, & Zemel, 2002). Inves-
useful in studies of pubertal development when
tigators emphasized that children and adolescents
precise estimates are required.
with Crohn's disease tend to be delayed in both
Three international studies examined agreement of
linear and pubertal development and that even
self-report and physical examinations for pubertal
though they are off-time from their healthy peers,
their perceptions are on target. In another study, 87
methods to collect age at menarche, nor were studies
boys and girls (aged 8 – 16 years) with type 1 or type 2
reported in the literature regarding reliability of age
diabetes were recruited to examine the accuracy of
at menarche across time or method. In the past,
self-report of puberty (Stephen, Bryant, & Wilson,
correlations ranged from .60 to .81 (Bergsten-Bruce-
2008). A physical examination was conducted, and
fors, 1976; Casey et al., 1991; Damon & Bajema, 1974;
adolescents independently viewed drawings of the
Livson & McNeill, 1962; Must et al., 2002; Susman &
pubertal stages. k coefficients were substantial (4.61)
Ponirakis, 1997) and were obtained in females across
for both genders. Age, metabolic control, race, type of
the teen years to the seventh or eighth decade.
diabetes, and BMI had no impact on accuracy of
Accuracy was hampered by longer time to recall
(Koo & Rohan, 1997) or socioeconomic factors
Based on the aforementioned studies, if one-to-one
(Artaria & Henneberg, 2000). In the future, it
agreement between self-report and physical exam-
would be helpful for studies to determine ways to
ination is required for research purposes, then self-
enhance reliability as well as to examine ‘‘accuracy''
reports may not be a valid and reliable measure. Many
or to report age at menarche across time in
of these studies had very low k coefficients, including
longitudinal studies. It is likely that age at
the study with a sample size of nearly 1,400 (Wu et al.,
menarche will continue to be the most frequently
2001). Also, in some subpopulations (i.e., obese), self-
used measure to determine timing of puberty in
report of pubertal stage may not be a reasonable
girls, and any method to enhance its reliability
alternative. Investigators may want to consider these
would be beneficial to the field.
newer studies when weighing their proposed meth-odology for staging, considering that large samples
were represented containing racial/ethnic diversityand that specific subgroups represented variability in
Sex steroids and adrenal androgens are the under-
weight and health issues. Two studies reported above
lying substrate of the external changes reflected by
appear to show that adolescents undergoing regular
pubertal stage. Here we review two important issues
care for a chronic illness may possess more knowledge
regarding measurement of pubertal hormones over
than others about how their disease affects growth and
the last decade. First, we discuss some of the meth-
development; in turn, their agreement was higher
odological advances pertaining to hormone assays
with clinician ratings than self-ratings reported in
and methods of collecting hormones. Second, we
other studies.
review the issue of comparing hormone concentra-tions to pubertal stage.
Agreement with different self-report methods.
9- to 16-year-old boys and girls (N 5 2,864), Bond
Methodology of hormone measurement.
et al. (2006) compared agreement between two
the last decade, some of the most important ad-
methods of self-report: the PDS and sexual matu-
vances in hormone measurement have involved
ration using line drawings and written descriptions.
perfecting blood spot and saliva assays and con-
k coefficients for males ranged from .13 to .36 in
ducting studies using these less invasive meth-
grades 5, 7, and 9, but the k was somewhat higher for
odologies in children and adolescents.
the full sample (k 5 .42). For girls, k coefficients were
Use of saliva samples for assaying hormone
lowest in grade 9 (.17 and .19 for pubic hair and
concentrations has gained more attention in recent
breast, respectively); k coefficients were .47 and .50
literature, which may be due to several factors. For
in the total sample. The investigators acknowledged
example, saliva samples are often easier and less
that comparisons of the two self-report measures did
expensive to collect than blood samples. However,
not include a comparison with the ‘‘gold standard''
the same issues exist for collection of both saliva and
of a physical examination by a health professional.
blood, depending on the specific hormone (e.g., time
Therefore, even with moderate k coefficients, it is
of day, number of samples, or day in menstrual cycle;
still not known whether the ratings were reflective of
see review in Dorn et al., 2006). Additionally,
degree of physical maturation. Importantly, the
salivary assays have been perfected and are more
study illustrates how two self-report measures can
readily available either by contract or by purchasing
provide different ratings and, in turn, impact the
assay kits for use in one's laboratory. Testing has
conclusion of a study.
played an important role in providing new assaysvia enzyme-linked immunosorbent assay (ELISA)
Self-report of age at menarche.
(e.g., androstenedione), thereby improving the
new information within the last decade regarding
PUBERTY AND ITS MEASUREMENT
conducting quality-control data and more normative
al., 2006). Thus, one cannot be sure that estradiol assays
data from different age and gender groups (Shirtcliff,
are sensitive enough for girls who are truly prepuber-
Granger, & Likos, 2002), and examining the impact
tal or for boys who are pre- or peripubertal. Since
of medication on hormone concentrations (Granger,
the Shirtcliff publication, a more sensitive assay
Hibel, Fortunato, & Kapelewski, 2009; Hibel, Granger,
for estradiol has been developed by a saliva analysis
Cicchetti, & Rogosch, 2007). Others have examined
company, but we remain unaware of any testing in
the reliability of concentrations of salivary steroids
pre- and peripubertal girls and boys in which pu-
based on the collection device used (Shirtcliff,
berty is documented by a research-grade physical
Granger, Schwartz, & Curran, 2001).
Blood spot analyses using finger stick method-
Assay sensitivity is particularly important for pre-
ology appeared less frequently in the literature with
and early pubertal boys and girls primarily with
biobehavioral studies in children and adolescents.
regard to gonadal steroids due to lower concen-
(For an exception, see Angold & Costello, 2006.) The
trations of pubertal hormones in these groups
method is relatively simple. Following the finger
(Grumbach & Styne, 2003). It is likely that pre-
stick, drops of blood are placed on special filter
pubertal concentrations of estradiol are below the
paper for later analysis. This methodology has advan-
detection level of the assay, particularly when using
tages in that only a small amount of blood is needed
radioimmunoassay and ELISA. Thus, in prepubertal
and storage of papers is easier than processing and
girls, concentrations may be undetectable in the
storage of tubes used in venipuncture. The most
majority of the group. Recently, a more reliable and
widely used blood spot tests in biobehavioral
valid serum method has been proposed: liquid
research include cortisol, progesterone, gonado-
chromatography tandem mass spectrometry (LC/
tropin, and estradiol concentrations.
MS-MS; Albrecht & Styne, 2007; Herold & Fitzgerald,
Some studies examined the reliability of blood
2003). Caution should be exercised when interpreting
spot analyses with serum and/or saliva samples. In
studies that do not use LC/MS-MS as the assay
a well-conducted study of adults, Shirtcliff, Reavis,
methodology in girls or boys in pre- and early
Overman, and Granger (2001) examined reliability
puberty (for testosterone and estradiol) and in girls
and sensitivity using blood spots for testosterone,
and women (for testosterone). Biro and Emans (2008)
estradiol, and progesterone. They reported high
illustrated this point in a recent editorial focusing on
correlations between serum samples and blood
PCOS and the interpretation of steroid hormone
spots but indicated limitations when measuring
concentrations. However, we encourage the reader to
progesterone and estradiol in men, likely due to
follow the literature closely because additional studies
low variability in those hormones.
may be published soon that utilize this newer
The reliability of serum, saliva, and/or blood spot
methodology for hormones that are changing duringpuberty is also an important issue. Estradiol increases
Comparing hormone concentrations to pubertal
during puberty in girls and boys, but the magnitude is
Some studies have opted to include pubertal
greater in girls. Estradiol measurement may be
hormones in their study not only to reflect puber-
challenging because of diurnal as well as monthly
tal development but also because hormones may
changes in girls, for the regularity of the cycle may
directly or indirectly influence the behavioral
not be predictable until several years after menarche.
or affective outcomes under study. For some it has
Thus, measuring estradiol pre- or peripubertally may
been tempting to consider measuring puberty-
be problematic. In a small sample of boys (n 5 17; aged
related hormones to indicate ‘‘stage of puberty''
8 – 9 years) and nonmenstruating girls (n 5 18; aged
rather than determining pubertal stage by physical
10.78 – 12.27 years), correlations of serum and blood
examination, especially because the former is
spot assays for estradiol were r 5.73 and .96,
thought to be less invasive. This is particularly true
respectively, whereas correlations between saliva and
when measuring hormones in saliva. However, most
blood spot assays were nonsignificant for boys
endocrinologists would agree that, in general, a
.18) and significant for girls (r 5.72) (Shirtcliff
reproduction-related hormone cannot be matched
et al., 2000). Investigators reported that the sensitivity
to a specific Tanner stage. Puberty-related hor-
of the salivary and blood spot analyses was adequate
mones show a wide range of concentration within
for most prepubertal girls and boys. However, as
stage and by gender. Further, there can be overlap
critiqued earlier, prepubertal was incorrectly equated
across stages. Depending on the hormone (e.g.,
with premenarcheal, and some of the nonmenstruating
morning testosterone), one sample may be able to
girls were likely in early or even mid-puberty (Dorn et
distinguish ‘‘prepubertal versus pubertal'' boys with
relative certainty if that concentration is high enough
between self-reported measures of puberty and
and is measured in the morning (Wu, Brown, Butler,
those obtained by physical examination. Overall,
Stirling, & Kelnar, 1993).
agreement between self-report and physical exam-
A recent important study has shed light on the
ination by k coefficients remains poor, and studies
issue of ‘‘comparability'' of pubertal stage and saliva
with participants who are obese observed even
hormone concentrations. Shirtcliff, Dahl, and Pollak
lower agreement. However, at least two studies in-
(2009) conducted a unique study in 160 boys and
dicated higher agreement by adolescents experienc-
girls aged 9 – 14 years in which they examined
associations of pubertal ratings by physical exam-
hypothesis that they may be more knowledgeable
ination, the PDS, and a picture-based interview
than some of their peers about how their bodies are
about puberty. The PDS was converted to a 5-point
developing or changing. With respect to pubertal
scale using a gonadal score (e.g., breast, menarche,
hormones, newer methodologies are in use that may
growth in height) and adrenal score to match Tanner
improve our understanding, particularly regarding
criteria. They determined associations of these three
the early stages of puberty. This area is still evolving
measures with salivary DHEA, testosterone, and
and therefore should be monitored to note progress.
estradiol. In comparing the physical examination
Although the last decade has revealed important
with the self-report using photographs and the
progress on the measurement of puberty and its
PDS, k coefficients were quite low and similar to
application across various studies, much remains
other studies (e.g., k 5 .29 – .43).
undone. Progress could be enhanced in various ways
The novel component of the study by Shirtcliff et al.
(see Susman & Dorn, 2009, for further elaboration).
(2009) is the comparison of hormone concentrations to
First, it would be beneficial to increase collaboration
the various pubertal stage ratings obtained by differ-
among developmental scientists and those in various
ent methodologies. The two measures of self-report
subspecialties of medicine, neuroscience, and statis-
were sometimes stronger correlates with hormones
tics as well as other areas of relevant technology (e.g.,
than was the physical examination. However, the
assay development, neuroimaging, computer pro-
statistical model predicting hormones was quite
gramming and usage). Such collaboration would
weak for girls, citing the limitation of estradiol based
allow more complex biobehavioral questions to be
on its cyclical nature (or lack thereof in some
addressed using appropriate and perhaps multiple
premenarcheal girls or those recently menarcheal).
measures of puberty. Timing and tempo of puberty
The model for boys was somewhat stronger. Without
should be included. In particular, data analytic
further methodological controls regarding the men-
strategies could enhance our understanding of pu-
strual cycle or change in sensitivity of the assay, the
berty or timing of puberty by incorporating use of
usefulness of estradiol in this sample is questionable.
latent constructs of puberty, growth curve modeling
Additionally, one must remember that salivary
with multiple samples at multiple time points, or
hormones were used in this study. Differences with
other appropriate strategies as exemplified in the
longitudinal study reported by Belsky et al. (2007).
empirically tested.
Second, studies of physiological or pathophysiolog-ical processes as well as studies of behavior couldincrease consideration and inclusion of the potential
THE NEXT DECADE: WHAT IS NEEDED?
relevance of puberty or timing of puberty to the
In the past decade, puberty has made the news! For
question at hand. For example, biobehavioral studies
example, new and exciting research has emerged
examining teenagers undergoing treatment for
regarding kisspeptin and the kisspeptin receptor and
asthma may benefit by including measures of pu-
their roles in initiation of puberty. Earlier timing of
berty. Such measures may explain a physiological
puberty continued to be documented, with some
reason for treatment success as well as a psychoso-
general indication that this secular trend may now be
cial reason for compliance with treatment. Third,
stable, particularly with respect to age at menarche.
studies are lacking on the structure and function
However, age at onset of puberty may continue to
of the brain in which puberty is determined by
decrease in populations in emerging countries where
research-grade physical examinations for staging.
resources are now more plentiful or with changes in
Romeo (2003) wrote a provocative review support-
social status. This past decade also introduced two
ing the notion that puberty is also a critical period
reviews on the importance of puberty and of mea-
‘‘. . of neural development that further organizes
suring puberty (Coleman & Coleman, 2002; Dorn
and shapes an organism's brain and behavioural
et al., 2006), and several studies reported agreement
potential'' (p. 1190). In many respects, this research
PUBERTY AND ITS MEASUREMENT
on puberty is in its infancy, and further development
puberty can provide insight into the reasons for the
regarding changes across puberty could contribute
observed earlier occurrence of puberty as well as
to our understanding of emotion, cognition, behav-
the contexts involved in these observations.
ior, and psychopathology. Fourth, diligence by re-viewers and editors in maintaining high standardsregarding measurement issues of pubertal status and
pubertal timing is necessary. We and others have
Aksglaede, L., Sorensen, K., Petersen, J. H., Skakkebaek, N.
articulated this need and have offered specific
E., & Juul, A. (2009). Recent decline in age at breast
suggestions (Dorn et al., 2006; Euling et al., 2008;
development: The Copenhagen Puberty Study. Pediat-
Susman & Dorn, 2009). Additionally, the newer,
rics, 123, e932 – e939.
more sensitive analytic techniques for assessment of
Albrecht, L., & Styne, D. (2007). Laboratory testing of go-
sex hormone levels should be utilized in serum
nadal steroids in children. Pediatric Endocrinology
hormone measurement. Fifth, more longitudinal
Reviews, 5(Suppl. 1), 599 – 607.
Angold, A., & Costello, E. J. (2006). Puberty and depres-
studies on timing and tempo of puberty are needed
sion. Child and Adolescent Psychiatric Clinics of North
as well as more studies in boys. Rigorous method-
America, 15, 919 – 937, ix.
ologies pertaining to measurement of puberty are
Artaria, M. D., & Henneberg, M. (2000). Why did they lie?
Socio-economic bias in reporting menarcheal age. Annals
Finally, with respect to timing of puberty, we
of Human Biology, 27, 561 – 569.
have indicated that numerous studies in the litera-
Banerjee, I., & Clayton, P. (2007). The genetic basis for the
ture look at varied outcomes in association with
timing of human puberty. Journal of Neuroendocrinology,
timing of puberty. Certainly, additional studies
19, 831 – 838.
need to be conducted, keeping in mind the use of
Baumann, D. A., Landolt, M. A., Wetterwald, R., Dubuis, J.
rigorous methodologies when measuring puberty
M., Sizonenko, P. C., & Werder, E. A. (2001). Psycho-
that are appropriate to the question. Virtually all
logical evaluation of young women after medical treat-ment for central precocious puberty. Hormone Research in
studies examining timing of puberty, regardless of
Pediatrics, 56, 45 – 50.
methodology of measurement, are summarized into
Belgorosky, A., Baquedano, M. S., Guercio, G., & Rivarola,
a global conclusion regarding puberty. We believe
M. A. (2009). Expression of the IGF and the aromatase/
that some of the studies using self-report would
estrogen receptor systems in human adrenal tissues
have been better served by conducting physical
from early infancy to late puberty: Implications for the
examinations for pubertal staging. Conclusions in
development of adrenarche. Reviews in Endocrine and
these studies regarding puberty may have been in-
Metabolic Disorders, 10, 51 – 61.
correct. Graber (2003) suggests that with respect to
Belsky, J., Steinberg, L. D., Houts, R. M., Friedman, S. L.,
puberty, we need to ‘‘. . move beyond demon-
DeHart, G., Cauffman, E., et al. (2007). Family rearing
strating effects, to better understanding of why ef-
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1302 – 1321.
Studies that examine timing of puberty and an
Bergsten-Brucefors, A. (1976). A note on the accuracy of
recalled age at menarche. Annals of Human Biology, 3,
outcome need to account for mechanisms (or me-
diators) as well as moderators that impact these
Biro, F. M., & Emans, S. J. (2008). Whither PCOS? The
associations and also to consider the context in
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Biro, F. M., Huang, B., Crawford, P., Lucky, A., Stiegel-
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La voz de los protagonistas Publicación Oficial de DAECPU Distribución Gratuita Diciembre de 2011 Año 7 Nº 278 Una casa en construcción y de puertas abiertas. / d / José AriSi. 14º Encuentro de Murga Joven / d / Adrián Baseda. Ya están las "reinitas" de Promesas.
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