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Puberty and Adolescent Sexuality

Frank M. Biro, MD; and Lorah D. Dorn, PhD
dolescence may be considered a time of reorganization of biological, cognitive, emotional, and social functioning.1 The biological changes that fall under the rubric of puberty include changes in the hypothalamic-pituitarygonadal axis, development of secondary sexual characteristics, increase in growth velocity, change in body composition, and attainment of fertility. Puberty consists of two independent but associated processes, adrenarche (an increase in adrenal androgens) and gonadarche (the reactivation of the hypothalamicpituitary-gonadal axis).2 This article explores the interrelationships between pubertal changes and adolescent sexuality.

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EDUCATIONAL OBJECTIVES

1. Describe the parameters of normal pubertal maturation. 2. Discuss the interactions between pubertal maturation and psychological change. 3. Explain the effects of the timing of maturation on physical, social, and psychological outcomes.

THE INITIATION OF PUBERTY The initiation (more accurately, the reinitiation) of puberty is not well dened. Why re-initiation? The luteinizing hormone releasing hormone (LHRH) pulse generator, a group of 1,500 to 2,000 neurons located within the basal hypothalamus, becomes active during fetal development; the gender differences during fetal life in the hypothalamic-pituitarygonadal axis arise from the greater levels of testosterone in the male.2 The decrease in placental estrogens during the second trimester leads to an increase in gonadotrophins and activation of the gonads and sex hormones in utero. This system remains active postnatally until approximately 6 months in boys and 12 to 24 months in girls. The inhibition of the LHRH pulse generator appears to be due to two mechanisms, the intrinsic central nervous system inhibitory system (the predominant mechanism) and the negative feedback from sex steroids.2 With the
Dr. Biro is professor of clinical pediatrics, Division of Adolescent Medicine, Cincinnati Childrens Hospital Medical Center, Cincinnati, OH. Dr. Dorn is professor of pediatrics, Division of Adolescent Medicine, Cincinnati Childrens Hospital Medical Center. Address reprint requests to: Frank Biro, MD; Division of Adolescent Medicine, Cincinnati childrens Hospital Medical Center, 3333 Burnet Ave., Cincinnati, OH 45229. The authors have no industry relationships to disclose.

onset of puberty, there is a disinhibition and reactivation of the LHRH pulse generator, although the mechanisms for these changes are unclear. Many have proposed leptin as an important mediator. Leptin is a polypeptide produced by adipose tissue and has a role in body weight homeostasis, reproduction, hematopoiesis, angiogenesis, and immune function. Leptin plays a central role in fat metabolism and signals the brains appetite centers and endocrine system regarding fat stores in the body. Some believe leptin inhibits

mass index (BMI; weight in pounds divided by height in inches divided by height in inches multiplied by 703) with total body fat and percent body fat; however, BMI also is correlated with fat-free mass.5 Annual increases in BMI during puberty, until age 16, are the result of increases in both fat-free mass (the greater portion) and total body fat (the lesser portion, especially in boys).6 There also are changes in the brain beyond those involved with the control and onset of puberty. For example, hormones may have different effects on the brain, depending on the devel-

The brain is a primary site for the modulation of multiple factors such as stress, nutritional signals, and exercise, which affect the emotional state and reproductive axis.
opmental stage. Irreversible changes in the structure and programming of the nervous system caused by the exposure to steroids during early development are called organizational effects, while those that lead to changes in behavior that are reversed if the hormone is removed are called activational effects.7 Functional correlates of changes in gray and white matter occur both before and after puberty.8 The brain is a primary site for the modulation of multiple factors such as stress, nutritional signals, and exercise, which affect the emotional state and reproductive axis.9 For example, acting through the hypothalamus and pituitary, stress triggers the secretion of the adrenal glucocorticoids, and repeated episodes of stress can lead to glucocorticoid hypersecretion. Howev-

neuropeptide Y and subsequently relaxes inhibition of the LHRH pulse generator,3 while others believe leptin to be a permissive factor necessary for the onset of puberty.2 Of note, leptin also could affect adrenarche; leptin stimulates 17hydroxylase and 17-20 lyase, two of the rate-limiting enzymes in the production of adrenal androgens.4 BIOLOGICAL CHANGES DURING PUBERTY As noted, during puberty, there are profound changes in body composition, including an increase in both total body fat and fat-free mass, with a greater increase in fat-free mass in boys than in girls.5 There is a high correlation of body

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er, the response to stress is different between men and women. Testosterone is a potent inhibitor of the responsiveness of the hypothalamic-pituitary-adrenal axis, whereas the inhibitory response is blunted in women, especially during the luteal phase of the menstrual cycle.10 An important point regarding brain development is that the area of the brain that integrates cognitive and affective information is among the later regions of the brain to mature completely, which may lead to differences between cool cognition and hot cognition.11 Dahl has dened cool cognition as that which occurs in calm settings (when one can carefully consider potential outcomes), in distinction to hot cognition, which occurs during conditions of strong emotions (such as high emotional or sexual arousal). Given the same adolescent with the same knowledge base, the outcomes may be very different in the same situation depending on whether cool cognition or hot cognition was used.11 Tempo, Timing, and Sequence of Puberty The three components in the assessment of pubertal maturation sequence, tempo, and timing may be relevant to adolescent sexuality. Multiple systems have been proposed for standardizing pubertal assessment; most health care providers use the Tanner rating system.12,13 More recently, Roede and van Wieringen14 published a set of photographs that depict the changes well. These descriptions (adapted from Marshall and Tanner) and photographs are shown in Figure 1, Figure 2 (see page 780), and Figure 3 (see page 781). Gonadal staging is less precise than pubic hair or breast staging;15,16 rather than assessing gonadal stage, the clinician should measure testicular volume, using an orchidometer.15 A cross-sectional study using data from participants attending primarily pediatric ofce settings in the United States

Stage 1

Stage 2

Stage 3

Stage 4

Stage 5

Stage 6

Figure 1. Stages in development of pubic hair in girls. Stage 1: Prepubertal with no pubic hair. Stage 2: Sparse, straight hair along the lateral vulva. Stage 3: Hair is darker, coarser, and curlier, extending over the mid-pubis. Stage 4: Hair is adult-like in appearance, but does not extend to the thighs. Stage 5: Hair is adult in appearance, extending from thigh to thigh. Stage 6 is no longer used commonly. (Figure reprinted with permission of author.14)

was published in 1997 and documented earlier onset of pubertal maturation in girls.17 Several other recent studies have conrmed these ndings, including data from the National Health Examination Survey,18 National Health and Nutrition

Examination Survey,19 Bogalusa Heart Study,20 and Fels Longitudinal Study.21 Much of this shift to younger ages at onset of puberty (and slightly lower age of menarche) appears to be secondary to the increase in body mass index (BMI)

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Stage 1

Stage 2

Stage 3

Stage 4

Stage 5 Figure 2. Stages in breast development in girls. Stage 1: Prepubertal, with no palpable breast tissue. Stage 2: Breast bud; elevation of the papilla and enlargement of areolar diameter. Stage 3: Enlargement of the breast, without separation of areolar contour from the breast. Stage 4: Formation of secondary mound above breast, from projection of areola and papilla. Stage 5: Recession of areola to contour of breast; papilla beyond contour of areola and breast. (Figure reprinted with permission of author.14)

in the US population.20,22 The trend in Europe is less well dened.23 A study of children in Greece appears to show

that both Greek boys and girls are undergoing earlier maturation, with more pronounced secular changes in girls.24

Additionally, this study showed a slight decrease in mean age of menarche, approximately 1 month per decade.25 A trend of earlier maturation in girls from Europe and the US was documented from the late 1800s through the 1950s26 and was attributed to overall improvement in socioeconomic conditions and general health.23,27-29 Some authors have suggested the more recent trends may be due to exposure to endocrine disruptors,30-32 including organochloride pesticides,33 or exogenous hormones in hair care products.34 However, it appears the most important factors contributing to earlier age of pubertal initiation include increases in calories and fast food consumption, decreases in physical activity, and increases in television viewing.35 With earlier onset of pubertal maturation and somewhat earlier age of menarche, it appears that onset of pubertal maturation and menarche may no longer be parallel,36,37 and the correlation between these two events has decreased during the past 50 years.37 In other words, these references state that the age of onset of puberty, and age of menarche, are no longer highly correlated. There are similar factors that lead to onset of both, but there are increasingly unique factors that contribute to onset of both. However, there also is controversy about the decrease in onset of puberty and menarche, and research on this topic is ongoing. Several studies have investigated the effects of timing of pubertal maturation on both physical and psychosocial outcomes. Some of these outcomes include shorter adult height and greater BMI in earlier maturing girls,38 but the greater effect may be on social and behavioral factors and provide a paradigm for the biopsychosocial model.39 This model proposes that social and environmental processes modify hormones and behaviors. The model suggests that there are both direct effects (such as biological development and behavior) and indirect

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effects (mediated or contextual developmental models) of puberty on outcomes.7 Earlier pubertal maturation appears to be generally advantageous for boys but disadvantageous for girls.1 Early maturation in girls is a risk factor for body image concerns40 and is associated with earlier initiation with sexual intercourse, although this may be mediated through afliation with older peers.41 In a longitudinal study evaluating the immediate and long-term effects of timing of pubertal maturation, Graber et al.42 found early maturation in girls led to higher rates of depression and substance use during adolescence. During adulthood, earlier maturers were more likely to have major depression and anxiety and had poorer adjustment skills and relationships; in contrast, late-maturing girls were more likely to have completed college by age 24. Both early and late maturing boys were at greater risk for subclinical psychopathology, although late maturers were less likely to be involved with substance use during adolescence. As adults, late maturing males had lower self esteem and were more likely to smoke and have substance abuse. Several authors have investigated changes in self-esteem in adolescents. Self-esteem generally increases in males during puberty.43 However, self-esteem in adolescent girls decreases during early puberty, although there appear to be differences between black and white girls.43 Additionally, self-esteem generally is stable throughout adolescence and into adulthood.44 During puberty, there appear distinct gender differences in rates of depression. Rates of depression before puberty are slightly greater in boys, but by midpuberty, rates in girls are approximately twice as great. The increased prevalence in females appears associated with serum levels of estrogen and testosterone.45 This sexual dimorphism may be mediated through the interaction of the sex hormones and the hypothalamic-pi-

Stage 1

Stage 2

Stage 3

Stage 4

Stage 5

Stage 6

Figure 3. Stages in development of pubic hair in boys. Stage 1: Prepubertal with no pubic hair. Stage 2: Sparse, straight hair along the base of the penis. Stage 3: Hair is darker, coarser, and curlier, extending over the mid-pubis. Stage 4: Hair is adult-like in appearance, but does not extend to the thighs. Stage 5: Hair is adult in appearance, extending from thigh to thigh. Stage 6 is no longer commonly used. (Figure reprinted with permission of author.14)

tuitary-adrenal axis.10 Testosterone is a potent inhibitor of the responsiveness of the hypothalamic-pituitary-adrenal

axis, but progesterone appears to blunt the inhibitory effect of estrogens, which may help account for mood changes

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Figure 4. Comparison of mean age of rst intercourse and rst marriage in US women, 1955 to 1980.

some women experience during the luteal phase (that is, the premenstrual syndrome).10 Additionally, estrogen has been shown to affect both serotonin synthesis and genes that effect serotonin transport and receptors.9 The discussion regarding the evaluation and management of delayed puberty is beyond the scope of this article, but other articles more adequately review the topic, including a recent case series.46 Hormonal Changes, Feelings, and Behavior The perspective of the adolescents storm and stress of the 19th century has become more moderate (the interested reader is referred to a recent review

by Arnett47). Several articles have examined the effects of hormonal changes on behavior. Changes in depression, aggression, delinquent behavior, and sexual activity have been attributed to changes in serum hormones that affect and are affected by changes in neurochemistry.1,9 For example, hormones appear to affect human sexuality; decreased serum levels of androgens lead to loss of libido in adult males, although the relationship of sex steroids and sexuality appears to be more complex in females. As reviewed by DeCherney,48 women who received estrogen alone had decreased sexual fantasies, while those who developed testosterone deciency following chemotherapy or surgery had decreased li-

Figure 5. Percentage of US high school students who have have sexual intercourse, 1991-2003.

bido and sexual responsiveness, which improved after testosterone replacement. Oral contraceptives have been noted to decrease libido, which may be the result of increased sex hormone binding globulin (decreasing free testosterone) and lowered luteinizing hormone (LH), which would decrease testosterone production in the ovary.48 There are other examples of the moderating effect of social and environmental processes on hormones and behaviors. Higher salivary testosterone levels were associated with greater likelihood of the initiation of sexual intercourse in adolescent boys, and those with higher concentrations had more frequent coital (and noncoital) sexual activity.49 Although testosterone also was associated with initiation of sexual intercourse in adolescent girls, the frequency of church attendance moderated the effect of testosterone.50 Two other studies reafrm the mediation of the effects of testosterone on behavior. Testosterone was related to adjustment problems, but the quality of the parentchild relationship decreased this association.51 Similarly, testosterone was related to nonaggressive symptoms of conduct problems in boys with deviant peers but it was related to leadership in boys with nondeviant peers, suggesting that testosterone was related to social dominance but that the specic behaviors differed by social context.52 Changes in timing of pubertal onset have a potential impact on timing of sexual initiation, as age of menarche is strongly associated with age at onset of sexual intercourse as well as with number of lifetime partners.53 As seen in Figure 4, the interval between age of rst intercourse and age at rst marriage has been increasing in the US. However, the slight but signicant delay in initiation of sexual activity, as shown in Figure 5, cannot be appreciated in Figure 4, given that the age of onset of sexual activity of adolescents included in the National Survey of Family Growth does not in-

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clude contribution from those who have not yet begun sexual activity. The healthcare provider of adolescents must protect the sexual health of patients, given the longer interval between sexual initiation and marriage. The promotion of abstinence is an important and necessary component of anticipatory guidance, particularly for preteens and young adolescents. For middle and older teens, the healthcare provider needs to engage in an active dialogue about reproductive health and include information about contraceptives to prevent unwanted pregnancies and sexually transmitted infections. For the sexually active teen or young adult, healthcare messages that include abstinence only

SIDEBAR.

Internet Resources for Adolescents, Parents, and Healthcare Providers

URL
http://www.itsyoursexlife.com http://www.iwannaknow.org http://www.nyacyouth.org http://www.siecus.org http://www.teenwire.com http://www.teenshealth.org

Provider
Kaiser Permanente American Social Health Association National Youth Advocacy Coalition Sex Information and Education Council Planned Parenthood Nemours Foundation

For the sexually active teen or young adult, healthcare messages that include abstinence only ... may lead, paradoxically, to a greater likelihood of pregnancy.
identity, and gender (sexual) orientation. Anatomic gender is the gender that one is assigned, typically on the basis of the apparent phenotype that is, phenotypic male or female. This may not always correspond to genotype sex. For example, phenotypic females with androgeninsensitivity syndrome (testicular feminization syndrome) have the 46, XY genotype but lack appropriate activity of the androgen receptor. Additionally, infants may be born with ambiguous genitalia (such as girls born with virilizing types of congenital adrenal hyperplasia, or boys born with severe forms of hypospadias). Gender identity is the sense of ones gender, or how one considers oneself as male or female. In addition to anatomic gender and gender identity is gender

(sexual) orientation, the physical and emotional attraction, as well as sexual fantasies, typically (but not invariably) directed toward one gender. SUMMARY Teenagers undergo biological, cognitive, and social changes. Each of these changes interacts with the other developmental parameters and may affect outcomes in late adolescence and adulthood. Sequence, tempo, and timing of puberty all affect when changes in hormones, feelings, and behavior will emerge in children. The pediatrician should recognize stages of pubertal development and be able to provide counseling and information to patients and parents. Some suggested resources are listed in the Sidebar. REFERENCES
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are provider-centered and not patientcentered care. This type of encounter may lead, paradoxically, to a greater likelihood of pregnancy (and infection) in the adolescent because of lack of disclosure and appropriate healthcare.54 ANATOMY, IDENTITY, AND BEHAVIOR Although issues of sexual identity are covered in greater depth in the article by Auslander et al. (see page 785), the reader should be familiar with the terms anatomic gender, gender (sexual)

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