Lifespan Development

Review article Transitions in Body and Behavior: A Meta-Analytic Study on the Relationship Between Pubertal Development and Adolescent Sexual Behavior Laura Baams, Ph.D. a,*, Judith Semon Dubas, Ph.D. a, Geertjan Overbeek, Ph.D. b, and Marcel A. G. van Aken, Ph.D. a aDepartment of Developmental Psychology, Utrecht University, Utrecht, the NetherlandsbResearch Institute of Child Development and Education, University of Amsterdam, Amsterdam, the Netherlands Article history: Received July 23, 2014; Accepted November 25, 2014 Keywords: Pubertal timing; Pubertal status; Adolescent; Sexual behavior; Sexual risk behavior; Meta-analysis See Related Editorial p. 580 ABSTRACT The present meta-analysis studies the relations of pubertal timing and status with sexual behavior and sexual risk behavior among youth aged 10.5 e22.4 years. We included biological sex, age, and ethnicity as potential moderators. Four databases were searched for studies (published between 1980 and 2012) on the relation between pubertal timing or status and sexual behavior. The outcomes were (1) sexual intercourse; (2) combined sexual behavior; and (3) risky sexual behavior. Earlier pubertal timing or more advanced pubertal status was related to earlier and more sexual behavior, and earlier pubertal timing was related to more risky sexual behavior. Further, the links between (1) pubertal status and combined sexual behavior and (2) pubertal timing and sexual intercourse status, com- bined sexual behavior, and risky sexual behavior were stronger for girls than boys. Most links be- tween pubertal status, timing, and sexual behavior and sexual risk behavior were stronger for younger adolescents. Moderation by ethnicity did not yield consistent results. There was signi ﬁcant variation in results among studies that was not fully explained by differences in biological sex, age, and ethnicity. Future research is needed to identify moderators that explain the variation in effects and to design sexual health interventions for young adolescents.

2015 Society for Adolescent Health and Medicine. All rights reserved. IMPLICATIONS AND CONTRIBUTION Research comparing the effects of pubertal status and timing across different sexual outcomes is lacking.

This meta-analysis gives a systematic overview of research examining these links. Early developing ad- olescents engage in earlier and more (risky) sexual behavior dthese effects were stronger for girls.

Recent perspectives on adolescent development view sexual development as a normative task of this life phase [1]. However, the early initiation of sexual behavior has also been linked with increased risk for unwanted pregnancies, sexually transmitted infections (STIs), and depression [2,3]. Given the obvious link between pubertal development and sexual reproduction capacity, the onset of puberty has been associated with the initiation of sexual desires and behavior. It is less clear to what degree pubertal development is related to sexual activity and whether early pubertal development is particularly problematic for the development of risky sexual behavior.

Although qualitative reviews and a large body of quantitative work have shown support for the relationship between pubertal timing and sexual development, no meta-analytic review exists that quanti ﬁes the magnitude of this relationship or that explains vari- ation in results across studies. Moreover, although most studies * Address correspondence to: Laura Baams, Ph.D., Department of Develop- mental Psychology, Utrecht University, Heidelberglaan 1, 3584CS Utrecht, the Netherlands. E-mail address: [email protected](L. Baams). www.jahonline.org 1054-139X/ 2015 Society for Adolescent Health and Medicine. All rights reserved.

http://dx.doi.org/10.1016/j.jadohealth.2014.11.019 Journal of Adolescent Health 56 (2015) 586 e598 focus on whether (vaginal) sexual intercourse has occurred, sexual development consists of a broad range of physical behaviors besides intercourse including activities such as kissing, petting, and oral sex.

The primary objective of the present meta-analysis is to examine and quantify the association between pubertal status and timing with nonrisky and risky coital and noncoital sexual behaviors.Not only do studies vary in terms of the sexual behaviors examined, but there is also substantial variation in how pubertal status and timing are assessed. Pubertal status is most often measured using (1) Tanner scale ratings made by a trained professional of adolescent pubic hair development (males and females), and breast development (females), or penis and testicular development (males); (2) adolescent self-report of these characteristics using photographs or line drawings; or (3) questionnaire measures of pubertal characteristics (growth spurt, acne, pubic hair, menarche, and voice change). Pubertal timing is often assessed using (1) adolescent self-report of age at growth spurt, age at the ﬁrst ejaculation, or voice change (males), or age at menarche (females); (2) age-adjusted measures of pubertal status (stage-normative); or (3) adolescent self- perceptions of whether their pubertal development is early, on time, or late (peer-normative). There is a moderate consistency across these different methods, however, the degree to which the adolescents rate themselves as more or less developed than their peers might not just re ﬂect their physical development but might also re ﬂect the degree to which they feel psychologically or behaviorally more mature [4e6] . Therefore, the second objective is to compare whether the magnitude of the association between pubertal development and sexual behavior and risky sexual be- haviors depends on how pubertal development was assessed. Drawing from a developmental systems approach which acknowledges that development in one domain (such as sexual development) does not occur independent from other domains (such as the social domain), we also examine whether the relation between pubertal and sexual development is also associated with individual differences in age, sex, or ethnic background. Previous research has shown that boys and girls show different patterns of pubertal development [7]and these differences are also suggested to relate to differences in social status and well-being [2,3,8e10 ] .

Therefore, in the present meta-analysis, we examine whether the effects of pubertal status and timing on sexual behavior and sexual risk behavior are different for boys and girls. Further, as adolescents move from a parent- to a peer-focused context during adolescence [11] , they are faced with more opportunities to engage in intimate and sexual behavior. Therefore, we also examine whether the effects of puberty on adolescents ’sexual development vary depending on the adolescents ’age. The link between pubertal development and sexual behavior might be stronger at younger ages, particularly in risky sexual behavior, because younger ado- lescents may not have the social and cognitive skills to engage in safer sexual behavior. However, stronger effects might also be found in older adolescents because they are less restricted by par- ents. Finally, research has shown several inconsistent racial and ethnic differences in pubertal [7,12]and sexual development [13,14] . Therefore, we examine whether these links are moderated by the ethnic background of adolescents.

The present study The primary objective of the present meta-analysis is to examine and quantify the association between pubertal status and timing with sexual behavior and risky sexual behavior. With this meta-analysis, we answer the following questions: Within the research literature published between 1980 and 2012, are pubertal timing and status related to sexual behavior and sexual risk behavior? If related, is this relation moderated by the way pubertal development is assessed (pubertal status or pubertal timing and stage-normative or peer-normative), or the age when pubertal development was assessed, sex, and ethnicity?

Although, initially our intention was to study differential effects of pubertal development on a range of sexual behaviors, most studies have examined either only sexual intercourse or have lumped together several sexual behaviors. Therefore, we have made the distinction between three sexual behavior categories as follows: (1) sexual intercourse status (had sexual intercourse or not) and age at the ﬁrst sexual intercourse; (2) combined sexual behavior (studies that include sexual intercourse andnoncoital sexual behaviors, in their combined measure of sexual behavior); and ( 3) sexual risk behaviors such as a combined measure of sexual risk behavior, unwanted pregnancy, contracting STIs or human immunode ﬁciency virus (HIV), noncondom/contraception use, and drug/alcohol use during sex.

Methods Sample of studies We searched four electronic databases (Scopus, MEDLINE, Web of Science, and PsycINFO) using variations and Boolean connectors of the key terms such as pubertal development, menarche, spermarche, spermatogenesis, breast development, adrenarche, gonadarche, oogenesis, adolescents, and sexual behavior. To supplement these searches, we searched reference lists of reviewed studies and contacted key authors in the ﬁ eld. To be included in the meta-analysis, studies had to be: (1) published in a peer-reviewed, English language journal; (2) empirically examined and reported the relation between pubertal development and adolescents ’(risky) sexual behaviors; (3) published between January 1980 and December 2012; and (4) must include adolescents with a mean age 24 years.

Information extracted from each study included: (1) age, sex, and/or ethnicity of sample; (2) pubertal development measure(s); (3) sexual behavior measure(s); and (4) effect size(s). Thirty percent of the studies were independently coded by two coders (including the ﬁrst author, L.B.). Intrarater reliability was good (correlations, .68 e.99). Any inconsistencies in the coding were checked by another independent coder and reconciled. Data were entered into SPSS 20.0 (SPSS Inc., Chicago, IL) and analyzed with the SPSS macro [15].

First, effect sizes were calculated or recoded using the Pearson product-moment correlation ( r) such that higher rvalues indicated a stronger relation between pubertal status, or timing, and (risky) sexual behavior. If a study reported results on group differences ( t, F , or odds/risk ratio), their results were converted to r[15] . Second, all r values were converted to the Fisher z(zr ). Third, for each effect size, we calculated a relative weight for zr,takingintoaccountthe sample size. To yield an interpretable overall effect size, the weighted mean effect size was then converted back to r(ES r).

Pubertal development Pubertal status. Several studies included self-report occurrences of physical pubertal events (e.g., the ﬁrst spontaneous nocturnal emission, menarche, Tanner drawings [16,17], Pubertal Develop- ment Scale (PDS) [18], Index of Adolescent Development, or L. Baams et al. / Journal of Adolescent Health 56 (2015) 586 e598 587 ratings of physical maturity by coders[19]) as markers of ado- lescents ’pubertal status. Some studies (k ¼5) reported using a pubertal status measure, in a sample of same-aged participants.

Using a measure of pubertal status among same-aged participants does not just assess how advanced someone is in their pubertal development, rather it creates a measure of pubertal timing by assessing how far advanced someone is in their pubertal devel- opment compared with their same-aged peers. Therefore, these studies were coded as using a pubertal timing measure.

Pubertal timing. Most studies used one of the following three ways to assess pubertal timing: (1) a self-report measure of adolescents ’ perceptions of pubertal timing (i.e., “Is your pubertal development early or late compared to peers? ”); (2) age at menarche; or (3) the PDS total score adjusted for age (that is, the total score was con- verted to a zscore within each age and gender group). Those studies that reported a comparison between early and on time (k ¼3), or on time and late (k ¼3) were also included and recoded such that a positive relation would indicate a stronger effect for the early (vs. on time) or the on time (vs. late) group. We classi ﬁed studies as using a “ stage-normative ”measure of pubertal timing on the basis of self- reported pubertal status (k ¼38), when for example, the PDS or physical ratings of adolescent ’s appearance was used. We classi ﬁed other studies as using a “peer-normative perceived ”measure of pubertal timing when youth reported on his or her perception of their own pubertal timing in comparison with peers (k ¼26). In our analyses, we tested whether the links to sexual behavior and sexual risk behavior were moderated by the measure of pubertal timing (stage-normative vs. peer-normative). We analyzed studies using age at menarche separately from the other studies.

Sexual development Sexual intercourse. All studies used a self-report measure of either age at the ﬁrst sexual intercourse or sexual intercourse status. Most studies did not de ﬁne sexual intercourse and if they did, they de ﬁned it as vaginal sexual intercourse. For the inclusion of studies under the category of sexual intercourse, they either had to use the term “ sexual intercourse ”or explain sexual intercourse as vaginal sexual intercourse. The studies that did not include sexual intercourse in their sexual behavior measure, or combined that with other sexual behaviors, were included under “combined sexual behavior. ” Combined sexual behavior. Several self-report measures were used to assess behaviors other than, or in addition to, sexual intercourse. Only six studies used a combined sexual behavior that did not include sexual intercourse. These studies used measures on self-reports of noncoital sexual behavior such as petting, kissing, caressing, and oral sex. There were 30 studies that used a combined measure of noncoital sexual behaviors andcoital sexual behaviors.

We grouped these two categories together (purely noncoital and combined coital and noncoital) into the combined sexual behavior measure. To explore whether the inclusion of purely noncoital (k ¼6) and combined coital and noncoital measures (k ¼30) made a difference in relation to pubertal development, we tested the moderation of these two forms of measuring combined sexual behavior. There was only one study [20]that reported on the link between pubertal development and individual (noncoital) sexual behavior (e.g., kissing and caressing), and therefore, we were un- able to do separate analyses on speci ﬁc behaviors.

Risky sexual behavior. Measures of risky sexual behavior included questions about unwanted pregnancy, contracting STIs/HIV, noncondom/contraception use, and drug/alcohol use during sex. Some studies included a measure of risky sexual behavior that comprised multiple risky behaviors. The number of studies examining different categories of risky sexual behavior measures was too small to analyze separately.

Moderators Age. For age, we included the mean age of the sample. If not reported, we took the median age of the reported range of ages.

Sex. Studies were classi ﬁed according to the sex composition of the sample: (1) boys; (2) girls; and (3) mixed. In our moderator analyses, we used dummy variables (boys vs. girls; mixed vs.

girls; and mixed vs. boys) to compare the different samples.

Ethnicity. Unfortunately, there were only two studies that reported results separately for ethnic groups other than black participants.

One study had results reported separately for white and Latina girls [13], the other only included Hispanic girls in their study [21].

Most studies include a wide range of ethnic backgrounds in their sample, with the most predominant ethnic groups being white or black/African American. Further, some studies reported results separately for white and black/African American adolescents.

Therefore, for the present study, we were only able to examine differences in the associations between pubertal development and sexual behavior and sexual risk behavior between black or white adolescents. Thus, for ethnicity, we included the percentage of “ black ”adolescents in the sample ifthis was reported. 1If, in a study, it was reported that a sample was 100% white, this was coded as 0% black participants. Enough studies were found to examine four relations as follows: pubertal status and pubertal timing with and sexual intercourse status; pubertal timing with combined sexual behavior; and age at menarche with age at sexual intercourse.

Data analyses To examine the heterogeneity of effect sizes across studies, we assessed the Q statistic. This statistic indicates the variability across effect sizes that may be explained by other sources and indicates the need to examine moderators, if this statistic is signi ﬁcant [15].We analyzed the data using ﬁxed effects models and random effects models. Because the present meta-analysis includes small samples of effect sizes, we only report the ﬁxed effects model results. 2We examined sex, age, and ethnicity of the sample, stage-normative versus peer-normative measure of pubertal timing, and purely noncoital combined sexual behavior versus combined sexual be- haviors that included coitus as potential moderators in the relation between pubertal status or timing and (risky) sexual behavior. The moderation analyses yielded bvalues those when signi ﬁcant indi- cate an interaction between the moderator and predictor (pubertal status or timing) in their effect on the sexual behavior outcomes.

Results Description of studies: overview of included studies Initially, 70 studies were found. In total, 50 independent studies met the inclusion criteria, with a total of 112 effect sizes. Tab le 1 1For the purpose of this meta-analysis, samples with black or African American adolescents are categorized as “black.” 2Results of the random effects models are available from the corresponding author on request.

L. Baams et al. / Journal of Adolescent Health 56 (2015) 586 e598 588 Table 1 Included studies and characteristicsPuberty measure Sexual behaviormeasureSex of sample Mean age Country Ethnicity N r Sexual intercourse (1) Arim et al., 2011 [22] Pubertal timing relative to peers on the basis of PDS Intercourse status (1) Boys 13 Canadad3,700 .03 (2) (2) Girls 3,564 .27 Benson et al., 1995 [23] Timing of age at menarche or the ﬁrst semen release Virginity loss (yes/no) 50% Boys; 50% Girls 13 U.S.A.

33% black 45% Hispanic 27% white 307 .32 Bingham et al., 1990 [24] Age at menarche Age at the ﬁrst sexual intercourse Girls 17 U.S.A. d1,717 .17 (1) Brown et al., 2006 [25] Pubertal timing relative to peers Sexual intercourse status (yes/no) at follow-up (2 years later) 50% Boys; 50% Girls 13.7 U.S.A.

(1) 100% black526 .13 (2) (2) 100% white491 .06 Campbell et al., 2005 [26] Pubertal status on the basis of secondary sexual characteristics, the ﬁrst erection, and ﬁ rst spontaneous nocturnal emission Intercourse status Boys 15 Zimbabwe100% black 437 .09 (1) Cavanagh, 2004 [13] Age at menarche Sexual intercourse statusGirls 13.88 U.S.A. (1) 100% white 882 .20 (2) U.S.A. (2) 100% Latina149 .40 (1) Crockett et al., 1996 [27] Pubertal timing relative to peers of the same age and gender Timing of the ﬁrst intercourse (early, middle, or late) (1) Girls 16.5 d 166 .06 (2) (2) Boys 123 .04 Deardorff et al., 2005 [28] Age at menarche Age at the ﬁrst sexual intercourse Girls 20.5 U.S.A. 13.8% black 31.4% Latina 28.7% Non-Hispanic white 23.9% Native 2.0% other 666 .27 (1) Deppen et al., 2012 [29] (1) Perception of pubertal timing (on time vs. early) on time is reference group Sexual intercourse before the age of 16 years Girls 18 Switzerland 18.1% parental non-Swiss origin 890 .20 (2) (2) Perception of pubertal timing (on time vs. late) on time is reference group 17.4% parental non-Swiss origin 778 .31 Durant et al., 1990 [21] Age at menarche Engaging in premarital coitusGirls 17 U.S.A. 100% Hispanic 202 .25 Edgardh, 2000 [30]Menarche 11 years Coitarche <15 years; coitarche >15 years Girls 17 Sweden d 712 .21 Edgardh, 2002 [31]Pubertal timing assessed with early puberty (the ﬁrst ejaculation before the age of 13 years) Intercourse status Boys 17 Sweden 13% Immigrant background647 .19 Felson and Haynie, 2002 [32] Pubertal status assessed with PDS items on pubic hair; facial hair; and voice changes. Items were summed. Sexual intercourse (yes/ no) Boys 14.1 U.S.A. 54% white 5,700 .20 Gaudineau et al., 2010 [33] Early menarche (before the age of 11 years) Sexual intercourse before the age of 5 years Girls 15 France d1,072 .20 Johnson and Tyler, 2007 [34] Pubertal status assessed with status question for boys and menarche onset question for girls Age at the ﬁrst sexual intercourse 52% Boys; 48% Girls 12.59 U.S.A.

d2,494 .11 ( continued on next page ) L. Baams et al. / Journal of Adolescent Health 56 (2015) 586 e598 589 Table 1 ContinuedPuberty measure Sexual behaviormeasureSex of sample Mean age Country Ethnicity N r Kahn et al., 2002 [35]Age at menarche Age at the ﬁrst sexual intercourse Girls 20.4 U.S.A. 59% white 12% black 13% Hispanic 9% Asian 7% other504 .16 Kim and Smith, 1999 [36] Age at menarche Age at the ﬁrst sexual intercourse Girls 19.5 U.K. d 228 .34 (1) Khurana et al., 2012 [37] Pubertal status assessed with Tanner drawings (boys, genitals and body hair; girls, breast and pubic hair) (1) Intercourse status 48% Boys; 52% Girls 13.4 U.S.A. 55% Non-Hispanic white 28% Non-Hispanic black 9% Hispanic347 .26 (2) (2) Intercourse status 1 year later .26 Koo et al., 2012 [38]Pubertal status (boys, questions about body and voice change; girls, questions about breast development and body hair). Intercourse status 45.1% Boys; 54.9% Girls 10.5 U.S.A.

99% African-American408 .26 (1) Kuzman et al., 2007 [39] (1) Age at menarche; on time compared to early Sexual intercourse before the age of 16 years Girls 15.5 Croatia d 656 .19 (2) (2) Age at menarche; Late compared to early 284 .31 (1) Kvalem et al., 2011 [40] Pubertal timing relative to peers at wave 1 Coital onset at wave 2 (2 years later) (1) Boys 14 Norway d1,246 .09 (2) (2) Girlsd1,343 .04 (3) Pubertal timing relative to peers at wave 2 Coital onset at wave 3 (5 years later) (3) Boys 15.6 d 598 .03 (4) (4) Girlsd662 .04 (1) Lam et al., 2002 [20] (1) Age at the ﬁrst emission ( ﬁrst conscious ejaculation) Sexual intercourse (yes/ no) Boys 16 Hong Kong d 1,905 .12 (2) (2) Age at menarche Girls 1,907 .06 (1) Meschke et al., 2000 [41] (1) Age at menarche Age at the ﬁrst sexual intercourse (age <16 years; age 16 years; inexperienced) Girls 16.5 U.S.A. 100% white 268 .28 (2) (2) Age at growth spurt Boys16.5 157 .12 (1) Michaud et al., 2006 [42] (1) Pubertal timing relative to peers; early versus average Sexually active Girls 18 Switzerlandd2,771 .18 (2) (2) Pubertal timing relative to peers; late versus average 2,314 .13 (3) (3) Pubertal timing relative to peers; early versus on time Boys 3,359 .16 (4) (4) Pubertal timing; relative to peers; Late versus on time 3,018 .15 Miller et al., 1997 [43] Age at menarche Age at the ﬁrst sexual intercourse Girls 20.5 U.S.A. 28.7% black 386 .06 Neberich et al., 2010 [44] Age at menarche Age at the ﬁrst sexual intercourse Girls 21.4 Germany d 381 .17 (1) Ostovic and Sabini, 2005 [45]Pubertal timing assessed with ages at several pubertal development events Intercourse status (1) Girls 21.8 U.S.A. 58.8% white 27% Asian or Asian-Indian 4.3% black 3.2% Hispanic 6.7% other141 .06 (2) (2) Boys22.4 124 .12 L. Baams et al. / Journal of Adolescent Health 56 (2015) 586 e598 590 Table 1 ContinuedPuberty measure Sexual behaviormeasureSex of sample Mean age Country Ethnicity N r Part et al., 2011 [46]Pubertal timing assessed with ages at menarche and spermarche Intercourse status 46.9% Boys; 53.1% Girls 15.5 Estonia d959 .17 (1) Phinney et al., 1990 [47] Age at menarche Age at the ﬁrst sexual intercourse Girls 17 U.S.A. (1) 100% black 581 .29 (2) (2) 100% nonblack1,253 .17 Rosenthal et al., 2001 [48] Age at menarche Age at initial sexual intercourseGirls 14.5 U.S.A. 78% black 22% white 143 .66 (1) Rosenthal et al., 1999 [49] Physical development timing (less or about as mature as peers vs. more mature than peers) Timing of sexual intercourse (early or late initiator) (1) Boys 16.6 Australia d 94 .20 (2) (2) Girls 147 .16 Spencer et al., 2002 [50] Pubertal timing assessed with ages at several pubertal development events Intercourse status 43% Boys; 57% Girls 12.5 U.S.A. 84% white 16% black188 .14 Vanoss Marín et al., 2000 [51] Menarcheal status Sexual intercourse (yes/no)Girls 11.5 U.S.A. 1,242 .19 Combined sexual behavior (1) Brown et al., 2006 [25] Pubertal timing relative to peers Precoital sexual activity (kissing eoral sex) at follow up (2 yrs later) 50% Boys; 50% Girls 13.7 U.S.A.

(1) 100% black526 .22 (2) (2) 100% white491 .08 (1) Campbell et al., 2005 [24] Pubertal status on the basis of secondary sexual characteristics, ﬁrst erection, and ﬁrst spontaneous nocturnal emission (1) Light petting Boys 15 Zimbabwe100% black 397 .19 (2) (2) Heavy petting 414 .12 (1) Flannery et al., 1993 [52] Pubertal status (Tanner line drawings) Sexual experience (kissed-intercourse) (1) Boys 13.5 U.S.A. 78% Caucasian parents 15% Hispanic parents376 .51 (2) (2) Girls 397 .53 (1) Hipwell et al., 2010 [53] Onset of menarche at the age of 11 years (yes/no) (1) None versus moderate sexually intimate behavior at the age of 12 years Girls 11.58 U.S.A. 54.8% African- American 39% European- American 6.2% multiethnic or belonging to another ethnic group 604 .18 (2) (2) Mild versus moderate sexually intimate behavior at the age of 12 years 581 .08 (1) James et al., 2012 [8] Pubertal maturation (combined measure incl PDS) at time 1 (grade 6). Recoded as pubertal timing a Timing of sexual debut at time 7 (grade 12) Average of ﬁrst sexual encounter, and ﬁrst sexual intercourse. Girls 11.86 U.S.A. 82% European- American 14% African- American 4% other129 .33 (2) Boys13.86 109 .17 (1) Lam et al., 2002 [20] Age at the ﬁrst emission ( ﬁ rst conscious ejaculation) (1) Kissing Boys16 Hong Kong d1,912 .11 (2) (2) Caressing 1,908 .11 (3) Age at menarche (3) Kissing Girls 1905 .10 (4) (4) Caressing 1,892 .09 (1) Meschke and Silbereisen, 1997 [54] Pubertal timing compared with peers Age at the ﬁrst personal sexual experience Girls 16.75 Germany (1) West Germany 227 .06 (2) (2) East Germany 128 .21 (3) Boys(3) West Germany 242 .06 (continued on next page ) L. Baams et al. / Journal of Adolescent Health 56 (2015) 586 e598 591 Table 1 ContinuedPuberty measure Sexual behaviormeasureSex of sample Mean age Country Ethnicity N r (4) (4) East Germany 105 .16 (1) Miller et al., 1998 [55] PDS pubertal timing (standardized) Sexual behavior (held hands-intercourse) (1) Boys 12.9 U.S.A. 95% white 152 .17 (2) (2) Girls 169 .13 (1) Negriff et al., 2011 [56] (1) Tanner breast/ genital at wave 1 Sexual activity summed across eleven activities at wave 1 53% Boys; 47% Girls 11 U.S.A.

38% African-American 39% Latino 12% Biracial 11% Caucasian 454 .23 (2) (2) Tanner pubic hair at wave 1 .20 (3) (3) PDS at wave 1 Sexual activity summed across eleven activities 1 year later .09 (4) (4) Tanner breast/ genital at wave 1 .23 (5) (5) Tanner pubic hair at wave 1 .20 (6) (6) PDS at wave 1 Sexual activity summed across eleven activities 2 years later .12 (7) (7) Tanner breast/ genital at wave 1 .09 (8) (8) Tanner pubic hair at wave 1 .06 (9) (9) PDS at wave 1 .08 (1) Ostovic and Sabini (2005) [45] Pubertal timing assessed with ages at several pubertal development events Age at the ﬁrst sexual arousal (1) Girls 21.8 U.S.A. 58.8% white 27.0% Asian or Asian-Indian 4.3% black3.2% Hispanic 6.7% other 148 .47 (2) (2) Boys22.4 129 .46 (1) Price et al., 2009 [57] Pubertal status at the age of 13 years assessed with Tanner line drawings Sexual behavior (oral and/or coital) at the age of 15 years (1) Girls 13 U.S.A. 90% European- American 4% African- American 2% Asian-American 2% Hispanic 2% Native American127 .15 (2) (2) Boys 110 .23 (1) Savin-Williams, 1995 [58] Age at pubertal onset (1) First homosexual sexual experienceBoys 20.9 U.S.A. d 71 .30 (2) (2) First heterosexual sexual experience 41 .07 (1) Smith et al., 1985 [59] (1) Pubic hair stage assessed with Tanner drawing. Sexual behavior (kissing-intercourse) Girls 13.5 U.S.A. 100% white 433 .93 (2) (2) Estrogen development assessed with a Tanner drawing of breast development and three items assessing perception of breast and hip development, and general “ curviness ”. .54 (3) (3) Pubertal status measured by 10 items Boys 378 .87 Van Ryzin (2011) [60] Physical maturity assessed with two items on body hair and skin changes.

Recoded as pubertal timing a Sexual experimentation(items on kissing e touching below the waist summed) 52% Boys; 48% Girls 14 U.S.A. 88% Euro-American 7% mixed ethnic background 2% Hispanic 1% African- American 1% Native American 1% Asian American363 .11 L. Baams et al. / Journal of Adolescent Health 56 (2015) 586 e598 592 Table 1 ContinuedPuberty measure Sexual behaviormeasureSex of sample Mean age Country Ethnicity N r (1) Van Zalk et al., 2011 [61] Pubertal status assessed with a partial PDS (1) Lifetime intercourse frequency (no e several times) wave 1 52% Boys; 48% Girls 13.73 Sweden 13% ﬁrst born immigrant 12.5% second born immigrant 750 .18 (2) (2) Lifetime intercourse frequency (no e several times) wave 2 .21 (3) (3) Impulsive sexual behavior (sleeping on the ﬁrst night) wave 1 .14 (4) (4) Impulsive sexual behavior (sleeping on the ﬁrst night) wave 2 .21 Risky sexual behavior Aruda, 2010 [62]Age at menarche Condom use Girls18 U.S.A. 36% Hispanic and 50.2% black 17% white 4% American-Indian .3% Asian 22% other305 .56 Belsky et al., 2010 [63] Age at menarche Risky sexual behavior at the age of 15 yearsGirls 12.5 U.S.A. 82% white 12% black 6% Hispanic526 .25 (1) Boden et al., 2011 [64] Age at menarche (1) Pregnant by the age of 18 yearsGirls 13.5 New Zealand d 497 .73 (2) (2) One or more STI by the age of 18 years .63 Durant et al., 1990 [21] Age at menarche Contraceptive behavior Girls 17 U.S.A. 100% Hispanic85 .25 (1) Halpern et al., 2007 [65] Pubertal timing relative to peers Sex for drugs or money (1) Boys 14 U.S.A. 79% white 14% black 7% other1,879 .03 (2) (2) Girls13.9 2,239 .33 (3) Combination sex and drug use (3)Boys 1,879 .13 (4) (4) Girls 2,239 .21 (1) Marceau et al., 2011 [66] (1) Tanner pubic hair Risky sexual behavior Boys 15.5 U.S.A. 100% white326 .03 (2) (2) Tanner genital development 326 .04 (3) (3) Tanner pubic hair Girls 340 .05 (4) (4) Tanner breast development 343 .04 (1) James et al., 2012 [8] (1) Pubertal timing at time 1 assessed with the PDS and IAD, partialling out age.

Recoded as pubertal timing a Risky sexual behavior6 years later Girls 11.86 U.S.A. 82% European- American 14% African- American 4% other129 .25 (2) (2) Pubertal timing at time 3 assessed with the PDS and IAD, partialling out age Risky sexual behavior 4 years later Boys 13.56 109 .02 Shew et al., 1994 [67]Age at menarche HPV infection (yes/no) Girls 17 U.S.A. 48% white 44% black 7% other208 .06 (1) Siebenbruner et al., 2007 [19] Physical maturity rated by coders at the age of 13 years. Recoded as pubertal timing a (1) High-risk versus sexual abstainers.

Sexual risk behavior at the age of 16 years.

Composed of number of sexual partners and contraception use. 54% Boys; 46% Girls 13 U.S.A. Mother ’s ethnicity:

86% Caucasian 10% African- American 4% Native American or Asian 118 .04 ( continued on next page ) L. Baams et al. / Journal of Adolescent Health 56 (2015) 586 e598 593 presents the included studies across the separate meta-analyses.

Samples included a total of 87,334 adolescents (min¼41, ma x ¼ 5,700). The mean ages of the adolescents in these studies ranged from 10.5 to 22.4 years, with an overall mean of 15.10 years (stan- dard deviation, 2.82). Of the included effect sizes, 51 were all girl samples, 32 were all boy samples, and 29 were mixed samples. Of these, most (k ¼71) were from the United States, see Ta ble 1.

Results of the separate meta-analyses In what follows, we show correlation effect sizes (ES r) that emerged from our meta-analysis, and whether the relations between pubertal development and sexual behavior and sexual risk behavior were moderated by pubertal timing measure, coital or noncoital sexual behavior measure, sex, age, and ethnicity of the sample (see Table 2for the overall effect size and heteroge- neity analyses). Only if the Q statistic was signi ﬁcant (heteroge- neity of effect sizes), was it necessary to conduct moderation results ( Table 3). For discontinuous moderators (sex, pubertal timing measure, and coital or noncoital behavior), we report the effect size and con ﬁdence intervals per group in Table 4. For continuous moderators, we report the bvalue of the moderation in Table 3 and the direction of effects in text.

Pubertal status and sexual behavior and risky sexual behavior Sexual intercourse. There was only one study that examined the link between pubertal status and age at sexual intercourse [34], and another that studied the link between menarcheal status and sexual intercourse status [51]. Both studies found a signi ﬁ- cant small positive association between status and sexual inter- course (ES r¼ .11 and ES r¼ .19, respectively). No further analyses were conducted using these studies.

With a meta-analysis on ﬁve effect sizes, the results showed a small to moderate positive link between pubertal status and intercourse status (ES r¼ .20). That is, adolescents who are more advanced in pubertal development were more likely to have had intercourse. Follow-up moderation analyses revealed that this Table 1 Continued Puberty measure Sexual behaviormeasureSex of sample Mean age Country Ethnicity N r (2) (2) Low-risk versus sexual abstainers.

Sexual risk behavior at the age of 16 years.

Composed of number of sexual partners and contraception use. 122 .07 IAD ¼Index of Adolescent Development; PDS ¼Pubertal Development Scale.

The included studies and study characteristics are presented in order of sexual behavior measure, and then in order of alphabet.

The numbers in front of the author list represent multiple effect sizes from the same study.

Puberty measure presents the pubertal timing or status measure used in the study; sexual behavior measure presents the measure that was used to assess sexual behavior or risky sexual behavior.

Sex of sample includes 100% boys (Boys), 100% girls (Girls), or a mix of boys and girls; percentages are denoted.

Mean age denotes the mean age of the sample included in the analyses; if the mean sample was not reported, the median age of the range was included in the analyses.

Country denotes the country in which the study was conducted. Ethnicity denotes the reported percentages of adolescents with ethnic backgrounds.

We included percentage of black/African American adolescents in the moderator analyses and the bold percentages represent the values included in the moderator analysis. N denotes the number of participants in the particular analysis. Recoded effect size denotes the recoded effect sizes to r.

aThe effect sizes by James et al. (2012) and Van Ryzin (2011) were categorized under pubertal timing eage at combined sexual behavior because their pubertal status measure was assessed in a group of young adolescents with a narrow age-range. The effect sizes by Siebenbruner (2007) were categorized under pubertal timing erisky sexual behavior because their pubertal status measure was assessed in a sample of adolescents with the same age. Table 2 Omnibus Q statistic for the separate meta-analyses NQ omnibus dfp kES (95% conﬁdence interval) Pubertal status Age at sexual intercourse a 2,494 ddd 1.11 (d) Sexual intercourse status a ,b 1,242 ddd 1.19 (d) Sexual intercourse status 7,2399.934.042 5.20 (.18e.22) Combined sexual behavior 6,0651,279.12 12<.001 13.42 (.39e.44) Pubertal timing Age at sexual intercourse 2,35518.42 6.005 7.21 (.17e.25) Sexual intercourse status 28,050163.19 18<.001 19.14 (.13e.15) Age at combined sexual behavior 1,3039.246.161 7.13 (.08e.19) Combined sexual behavior 9,61065.2918<.001 19.14 (.12e.16) Risky sexual behavior 10,049133.08 11<.001 12.16 (.14e.18) Age at menarche Age at sexual intercourse 7,77979.2112<.001 13.21 (.19e.23) Sexual intercourse status 4,21231.99 4<.001 5.15 (.11e.18) Combined sexual behavior 4,9824.373.225 4.10 (.08e.13) Risky sexual behavior 2,118192.49 5<.001 6.51 (.48e.54) aWe were unable to test heterogeneity of effect sizes because only one study could be included for this analysis.bThis category includes the link of menarcheal status and sexual intercourse status, but has been categorized under pubertal status. L. Baams et al. / Journal of Adolescent Health 56 (2015) 586 e598 594 link was weaker for samples with a higher percentage of black adolescents.

Combined sexual behavior.With a meta-analysis on 13 effect sizes, we found a moderate to large positive association between pubertal status and combined sexual behavior (ES r¼ .42).

Adolescents who are more advanced in pubertal development were more likely to be engaged in sexual behavior. Moderation analyses indicated that this link was much stronger for girls than boys and mixed-sex samples. In contrast, this link was stronger for boys compared to mixed-sex samples. Further, this link was stronger for younger samples. There was no moderation by type of combined sexual behavior (coital or noncoital).

Pubertal timing and sexual behavior and risky sexual behavior Sexual intercourse. With a meta-analysis on 19 effect sizes, we found a small positive association between pubertal timing and sexual intercourse status (ES r¼ .14). Adolescents with an early pubertal timing were more likely to be engaged in sexual inter- course. Moderation analyses revealed that this link was much stronger for girls than boys, and much stronger for mixed-sex samples than boys. Further, this link was somewhat stronger for studies that used a stage-normative pubertal timing measure compared with a peer-normative pubertal timing measure, although this difference is small to medium.

With a meta-analysis on seven effect sizes, we found a small to moderate positive association between pubertal timing and age at sexual intercourse (ES r¼ .21). Adolescents with an early pubertal timing engaged in sexual intercourse at a younger age. This link was stronger for older adolescents but there was no moderation by pubertal timing measure (peer-normative vs. stage-normative).

Combined sexual behavior. With a meta-analysis on 19 effect sizes, we found a small positive association between pubertal timing and combined sexual behavior status (ES r¼ .14). Adolescents with Table 3 Moderating effects of gender, age, and ethnicity for the different meta-analyses Moderator Sex Age a Ethn. b PTc Coital d Boys (0) versus girls (1)Mixed (0) versus girls (1) Boys (0) versus mixed (1) Pubertal status Age at sexual intercourse e dd ddddd Sexual intercourse status e ,f dd ddddd Sexual intercourse status dd ns ns .71* dd Combined sexual behavior .35***.73*** .49*** .35*** dd ns Pubertal timing Age at sexual intercourse nsdd .76***d nsd Sexual intercourse status .40***ns .26*nsns.33***d Age at combined sexual behavior g dd ddddd Combined sexual behavior .39* .42** ns .25* ns ns ns Risky sexual behavior .70*** .60*** ns .40*** d .29* d Age at menarche Age at sexual intercourse dd d .27* .38** dd Sexual intercourse status dd d .63*** ddd Combined sexual behavior g dd ddddd Risky sexual behavior dd d .15* ddd Dashes represent moderator analyses that could not be tested because of lack of variance or nonreport of moderator.

Coital ¼combined sexual behavior measure includes coital or does not include coital behaviors; Ethn. ¼ethnicity; ns ¼not signi ﬁcant; PT ¼Pubertal timing measure. aPositive values indicate stronger relations for older youth. Negative values indicate stronger relations for younger youth.bPositive values indicate stronger relations for samples with a higher percentage of black adolescents. Negative values indicate stronger relations for samples with a lower percentage of black adolescents.

c0 ¼ Peer-normative pubertal timing; 1 ¼stage-normative pubertal timing.d0¼ Exclusively noncoital; 1 ¼coital.eWe were unable to test moderation effects because only one study could be included for this analysis.fThis category includes the link of menarcheal status and sexual intercourse status but has been categorized under pubertal status.gWe were unable to test moderator effects because there was no heterogeneity in effect sizes.

p > .05; * <.05; ** <.01; *** <.001. Table 4 Effect sizes and con ﬁdence intervals for signi ﬁcant categorical moderators Moderator Sex Pubertal timing measure Boys Girls Mixed Peer-normative Stage-normative Pubertal status Combined sexual behavior .48 (.44e.51) .72 (.69e.74) .19 (.15e.22) dd Pubertal timing Sexual intercourse status .11 (.09e.13) .17 (.15e.19) .16 (.12e.20) .13 (.11e.14) .15 (.13e.17) Combined sexual behavior .13 (.10e.16) .29 (.19e.40) .15 (.12e.17) dd Risky sexual behavior .07 (.04e.10) .24 (.21e.26) .05 ( .07 to .18) .18 (.16e.20) .06 (.01e.10) Dashes represent moderator analyses that could not be tested because of lack of variance or nonreport of moderator, or where differences were not signiﬁ cant.

L. Baams et al. / Journal of Adolescent Health 56 (2015) 586 e598 595 an early pubertal timing were more likely to be engaged in sexual behavior. Moderation analyses revealed that this link was much stronger for girls than mixed-sex samples and compared to boys, and stronger for older adolescents. There was no moderation by type of combined sexual behavior (coital vs. noncoital) and no moderation by pubertal timing measure (peer-normative vs.

stage-normative).With a meta-analysis on seven effect sizes, we found a signi ﬁ- cant small positive association between pubertal timing and age at the ﬁrst sexual behavior (ES r¼ .13; no heterogeneity of effect sizes). That is, adolescents with an early pubertal timing were more likely to engage in their ﬁrst sexual experience at a younger age.

Risky sexual behavior. With a meta-analysis on 12 effect sizes, we found a small positive association between pubertal timing and risky sexual behavior status (ES r¼ .16). Adolescents with an early pubertal timing engaged in more risky sexual behavior. This link was much stronger for girls than boys and mixed-sex samples.

This link was also stronger for younger adolescents and much stronger when a peer-normative pubertal timing measure was used, compared with when objective stage-normative pubertal timing measure was used.

Age at menarche and sexual behavior and risky sexual behavior Sexual intercourse. With a meta-analysis on 13 effect sizes, we found a small to moderate positive association between age at menarche and age at sexual intercourse (ES r¼ .21). Adolescents with a younger age at menarche engaged in sexual intercourse at a younger age. Moderation analyses revealed that this link was stronger for younger adolescents and for samples with a higher percentage of black adolescents. There were only ﬁve effect sizes that examined the link between age at menarche and sexual intercourse status. We found a small positive association that showed that adolescents with a younger age at menarche were more likely to have engaged in sexual intercourse (ES r¼ .15). This link was stronger for younger adolescents. Of these ﬁve studies, three did not report ethnicity of the sample and two examined the link be- tween age at menarche and sexual intercourse status separately for Latina and Hispanic girls. The mean effect size of these latter two studies separately also showed a small positive association (ES r¼ .07; 95% conﬁ dence interval [.04 e.12]; p< .001).

Combined sexual behavior. Only four effect sizes examined the link between age at menarche and combined sexual behaviord these showed a signi ﬁcant small positive association (ES r¼ .10 ; no heterogeneity of effect sizes). Adolescents with a younger age at menarche were more likely to engage in combined sexual behavior.

Risky sexual behavior. Only six effect sizes examined the link be- tween age at menarche and risky sexual behavior. We found a large positive association that showed that adolescents with a younger age at menarche were more likely to engage in risky sexual behavior (ES r¼ .51). This link was stronger for younger adolescents.

Discussion With the present study, we show the ﬁrst meta-analytical results of the relation between pubertal development and adolescent sexual behavior. Our results indicated that those adolescents with an early pubertal timing engaged in earlier, more advanced, and more risky sexual behavior. Also, those adolescents with a more advanced pubertal status engaged in earlier and more advanced sexual behavior.

Moderation of the relation between puberty and (risky) sexual behavior The present meta-analysis showed that the links of pubertal status and timing with nonrisky and risky sexual behavior were more pronounced in girls. The effect of pubertal status on com- bined sexual behavior showed a strong effect for girls but only a moderate effect for boys. The effect of pubertal timing on risky sexual behavior was moderate for girls and only small for boys.

This suggests a different mechanism by which puberty is related to sexual development for boys and girls. Overall, the results showed that, especially among young participants, (risky) sexual behavior was affected by a more advanced pubertal status, earlier pubertal timing, and a younger age at menarche. This may be because young adolescents are not as capable to handle potentially risky situations [68]or because they have a delay in the development of the cognitive control system of the brain [69,70]. In contrast, older adolescents are thought to have more opportunities to engage in sexual behavior, possibly because they experience fewer parental restrictions [71,72] .

Moderation by ethnicity showed inconsistent ﬁndings. For pubertal status measures that re ﬂect thelarche, andrenarche, and gonadarche, stronger links for white adolescents are found, whereas for the later-occurring menarche, stronger effects for black girls are found. The difference between pubertal status and age at menarche is important to consider because this indicates that pubertal status may show a combined effect of the development of several secondary sex characteristics, whereas menarche is the ﬁnal stage of girls ’pubertal development and an indicator of gonadarche. The present ﬁndings indicate ethnic differences in the magnitude of the link between pubertal development and sexual development, but especially, that research needs to disentangle the effects of thelarche, andre- narche, and gonadarche, and how these processes during adolescence may affect ethnic groups differently.

Finally, we examined whether including a stage-normative or peer-normative measure of pubertal timing moderated the links between pubertal timing and sexual behavior and sexual risk behavior. For the link between pubertal timing and sexual in- tercourse status, we found a small difference dthe effect of pubertal timing on sexual intercourse status was stronger when a stage-normative measure of pubertal timing was used. In contrast, for the link between pubertal timing and risky sexual behavior, we found a larger difference, and here the effect was stronger when a peer-normative measure was used. Our ﬁndings suggest that in predicting sexual risk behavior, the perception of one ’s pubertal timing may be even more important than the assessment of certain physical characteristics. This may indicate that when adolescents perceivetheir own pubertal development as “early ”relative to peers, they will also be psychologically geared toward more older, and/or more deviant social contexts [73] , or this may make them more vulnerable to the in ﬂuences of such contexts (contextual ampli ﬁcation; [68]), thereby increasing their chances of engaging in sexual risk behavior.

Given that very few studies include both peer-normative and stage-normative perceptions of pubertal timing in the same L. Baams et al. / Journal of Adolescent Health 56 (2015) 586 e598 596 study, it is impossible to tease apart whether peer-normative puberty overrides stage-normative pubertal timing in predict- ing sexual behavior or whether two different mechanisms are operating as follows: a biological mechanism that promotes sexual debut and a psychological one that promotes behavioral risk.

Pubertal status versus pubertal timingThree issues arise when comparing pubertal status to pubertal timing measures. First, several studies use a pubertal status measure in a sample of same-aged adolescents. Empiri- cally speaking, if pubertal status is assessed in such a sample, this automatically re ﬂects pubertal timing. Fortunately, we were able to account for this in the present meta-analysis by categorizing such studies as pubertal timing. However, it is clear that even among researchers, the distinction between pubertal status and pubertal timing is not always evident and, in addition to the assessment measure used, also depends on other factors. These include the age of the participants in the study, whether pubertal status scores are standardized, and whether age is controlled for in the analyses. Second, pubertal status and timing are con- founded dthose with an earlier pubertal timing have moved through more stages of pubertal development (which would indicate a more advanced pubertal status). In contrast, those with a later pubertal timing have not moved through as many stages, and are thus categorized as having a less advanced pubertal status. Considering these confounds, it is dif ﬁcult to interpret unique effects of pubertal status and timing from general age-related changes [74]. Third, studies on pubertal development often combine several physical changes (such as pubic hair and breast development, or pubic hair and growth spurt) into one pubertal status or timing measure, regardless of their biological basis [75]. Finally, with this meta-analysis it becomes clear that the only way to distinguish pubertal status from timing is with a longitudinal study, accounting for indi- vidual differences in status, timing, and rate of development [76].

Strengths and limitations With the present meta-analysis, we were able to quantify the effects of pubertal development on sexual behavior and sexual risk behavior with a large number of participants and across a wide range of ages. Although we were able to identify several gaps in the literature and provide a quantitative meta-analysis on the relation between pubertal development and sexual behavior, there are several limitations to this meta-analysis and the studies included to note. First, the measurement of pubertal development and sexual behavior was primarily by self-report and some were retrospective, which can be biased [5,77]. Second, we categorized studies on the basis of what they reported in the papers as their measures. Unfortunately, many studies do not clearly report the pubertal development measure, nor do many studies report whether they controlled for sex or age in their measure or ana- lyses. In addition to these methodological limitations to the studies, the present meta-analysis is limited in its conclusions about ethnicity. We were unable to include moderation by ethnicity other than percentage of black/African American par- ticipants. Such a measure gets at an indirect measure of whether the link between pubertal developments varies when more or less members of an ethnic group are included in the sample, but the magnitude of the actual relation between pubertal development and sexual behavior cannot be estimated. Our meta-analysis un- derscores two points as follows: (1) the need for investigators to report their analyses separately by ethnic group and (2) more research on pubertal and sexual development among different ethnic groups is needed and oversampling of these groups within strati ﬁcation samples may be necessary to achieve suf ﬁcient po- wer and reliability of the results.

Future research and implications The present meta-analysis suggests that puberty affects boys and girls differently, or that the environment reacts differently to their physical changes. To extend these ﬁndings even further, both for girls and boys, studies need to incorporate the social context into their research. Pubertal and sexual development do not occur in a vacuum dreactions from peers concerning the adolescents ’changing body, the relational context of sexual behavior, and availability of sexual health care all interact to affect adolescent sexuality. Further, our ﬁndings on sexual risk behavior among early maturing adolescents d strengthened by the idea that, when adolescents engage in sexual behavior at young ages, they tend to engage in more risky behaviors [78]d emphasize the need for early interventions to prevent pregnancy and STIs/HIV. Our ﬁndings underline the important role of an early transi- tion to reproductive maturity for the onset and timing of sexual and risky sexual behavior that is stronger for girls than boys. To study adolescent sexual development with a developmental systems approach, hormonal, genetic, and environmental factors need to be included.

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