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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.
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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.
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International Journal of Systematic and Evolutionary Microbiology (2013), 63, 893–899 Pseudonocardia antitumoralis sp. nov., adeoxynyboquinone-producing actinomyceteisolated from a deep-sea sediment Xin-Peng Tian,1 Li-Juan Long,1 Su-Mei Li,1 Jing Zhang,1 Ying Xu,2Jie He,2 Jie Li,1 Fa-Zuo Wang,1 Wen-Jun Li,2 Chang-Sheng Zhang1and Si Zhang1 1Key Laboratory of Marine Bio-resources Sustainable Utilization, CAS; RNAM Center for Marine