Secondary Sexual Characteristics in Boys: Data Fromthe Pediatric Research in Office Settings Network

WHAT’S KNOWN ON THIS SUBJECT: Recent investigations ofpubertal onset in US girls suggest earlier maturation. Thesituation for US boys is unknown, and existing investigations areoutdated and lack information on a key physical marker of malepuberty: testicular enlargement.

WHAT THIS STUDY ADDS: US boys appear to be developingsecondary sexual characteristics and achieving testicularenlargement 6 months to 2 years earlier than commonly usednorms, with African American boys entering Tanner stages 2 to 4earlier than white or Hispanic boys.

abstractBACKGROUND: Data from racially and ethnically diverse US boys areneeded to determine ages of onset of secondary sexual character-istics and examine secular trends. Current international studies sug-gest earlier puberty in boys than previous studies, following recenttrend in girls.

METHODS: Two hundred and twelve practitioners collected Tannerstage and testicular volume data on 4131 boys seen for well-childcare in 144 pediatric offices across the United States. Data wereanalyzed for prevalence and mean ages of onset of sexual maturitymarkers.

RESULTS:Mean ages for onset of Tanner 2 genital development for non-Hispanic white, African American, and Hispanic boys were 10.14, 9.14,and 10.04 years and for stage 2 pubic hair, 11.47, 10.25, and 11.43 yearsrespectively. Mean years for achieving testicular volumes of $3 mLwere 9.95 for white, 9.71 for African American, and 9.63 for Hispanicboys; and for $4 mL were 11.46, 11.75, and 11.29 respectively. AfricanAmerican boys showed earlier (P, .0001) mean ages for stage 2 to 4genital development and stage 2 to 4 pubic hair than white andHispanic boys. No statistical differences were observed betweenwhite and Hispanic boys.

CONCLUSIONS: Observed mean ages of beginning genital and pubichair growth and early testicular volumes were 6 months to 2 yearsearlier than in past studies, depending on the characteristic and race/ethnicity. The causes and public health implications of this apparentshift in US boys to a lower age of onset for the development ofsecondary sexual characteristics in US boys needs further exploration.Pediatrics 2012;130:e1058–e1068

AUTHORS: Marcia E. Herman-Giddens, PA, MPH, DrPH,a

Jennifer Steffes, MSW,b Donna Harris, MA,b Eric Slora,PhD,b Michael Hussey, MS,c Steven A. Dowshen, MD,d

Richard Wasserman, MD, MPH,b,e Janet R. Serwint, MD,f,g

Lynn Smitherman, MD,h,i and Edward O. Reiter, MDj

Departments of aMaternal and Child Health, and cBiostatistics,Gillings School of Global Public Health, University of NorthCarolina at Chapel Hill, Chapel Hill, North Carolina; bPediatricResearch in Office Settings, Department of Research, AmericanAcademy of Pediatrics, Elk Grove Village, Illinois; dDepartment ofPediatrics, Alfred I. DuPont Hospital for Children, Wilmington,Delaware; eDepartment of Pediatrics, University of Vermont,College of Medicine, Burlington, Vermont; fDepartment ofPediatrics, Johns Hopkins University, School of Medicine,Baltimore, Maryland; gContinuity Research Network, AcademicPediatric Association, McLean, Virginia; hChildren’s Hospital ofMichigan, Wayne State University School of Medicine/DetroitMedical Center, Detroit, Michigan; iNMA PedsNet, National MedicalAssociation, Silver Spring, Maryland; and jBaystate Children’sHospital, Tufts University School of Medicine, Springfield,Massachusetts

KEY WORDSsecondary sexual characteristics, growth and development,Tanner staging, testicular volume, PROS, secular changes,puberty

ABBREVIATIONSAAP—American Academy of PediatricsCI—confidence intervalHHANES—Hispanic Health and Examination SurveyNHANES—National Health and Nutrition Examination SurveyPROS—Pediatric Research in Office SettingsSSCIB—Secondary Sexual Characteristics in Boys

Dr Herman-Giddens is the principal investigator and primaryauthor; Dr Reiter is the co-principal investigator; Dr Reiter, MsSteffes, Ms Harris, Dr Slora, and Dr Wasserman have madesubstantial contributions to the conception and design of thisstudy, the acquisition of data, participated in drafting andcritically revising this article for intellectual content, and givenfinal approval of the version to be published; Mr Hussey, DrSerwint, and Dr Smitherman have made substantialcontributions to the analysis and interpretation of data,participated in drafting and critically revising this article forintellectual content, and given final approval of the version to bepublished; and Dr Dowshen has made substantial contributionsto the conception and design of this study, interpretation ofdata, participated in drafting and critically revising this articlefor intellectual content, and given final approval of the version tobe published.

(Continued on last page)

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The secular trend towarda youngerageof onset of puberty in girls in manycountries is now generally accepted.1–3

An expert panel convened in 2003 bySerono Symposia International, Inc,concluded that US girls were enteringpuberty at an earlier age than 40 yearsago.1 One of the key studies leading tothis conclusion, conducted by theAmerican Academy of Pediatrics (AAP),found girls were typically developingabout a year earlier than previouslyassumed.4 For boys, the panel con-cluded secular evidence was in-sufficient and further studies wereneeded. The most recent data on USboys comes from several analyses ofthe National Health and NutritionExamination Survey (NHANES) III 1988–19941,5–7; however, the data are 20years old, the accuracy of thegenital staging has been questioned,and testicular volumes were notobtained.5,8,9 No recent studies repre-sentative of US boys or with largenumbers in varied locales have beenpublished. Data on male puberty aremore difficult to obtain than femaledata because of the absence of aneasily determined marker, such asmenarche. Male pubertal stages areharder to assess visually than girls’stages, and orchidometry, an intrusiveprocedure, is not part of well-childexams.

Consequently, the AAP’s PediatricResearch in Office Settings (PROS)practice-based research network un-dertook this cross-sectional study todetermine the current ages of onset ofsexual maturity stages 2 to 5 and earlytesticular volumes in US boys seen forwell-child care and to assess whetherthere has been a shift in what is seen inoffice practice as compared with olderstudies. Puberty is complex, includingmany dynamic components. This studywas designed to report only physicalchanges, and not hormonal or otherchanges.

METHODS

Characteristics of PracticeParticipants

Clinicians were recruited from PROSpractices, the National Medical Asso-ciation Pediatric Research Network,and the Academic Pediatric Associa-tion’s Continuity Research Network.Participating clinicians comprised 196(93%) pediatricians, 1 family medicinephysician, and 15 (7%) nurse practi-tioners. Practices from 41 states and 1Canadian province enrolled subjectsbetween July 2005 and February 2010.Seventeen percent of practices werelocated in the Midwest, 24% in theNortheast, 31% in the South, and 28% inthe West. Approval was obtained fromthe AAP’s Institutional Review Boardand 54 local institutional review boardsaffiliated with participating practices.

Data Collection Process

Before the main study, Secondary Sex-ual Characteristics in Boys (SSCIB), weestablished trained clinicians’ inter-rater reliability for Tanner staging andorchidometry.10 Tanner staging is a 5-stage visual method for assessingdevelopment of secondary sexualcharacteristics (genital and pubic hairgrowth for males) from prepubertal(stage 1) to fully mature (stage 5).11

Using the study training manual,12

participating clinicians learned Tannerstaging and how to use a Praderorchidometer modified to contain onlythe 1-mL to 4-mL beads. Cliniciansdemonstrated competency by passinga question-and-photograph qualifyingexamination. Intraclass correlations inthe clinical setting, where 2 practi-tioners in 8 practices rated a total of 79boys, ranged from 0.61 for left testissize to 0.94 for pubic hair stage (allsignificant at P, .001), which indicatemoderate to substantial agreementdepending on the variable being mea-sured.10 For the main study, SSCIB, 212qualifying clinicians screened boys 6

through 16 years of age presenting forwell-child care for eligibility; each en-rolled up to 30 consecutive boys (15 from6–12 years of age and 15 from 13–16)from English- or Spanish-speaking fami-lies. Informed consent was obtainedfrom parents/guardians and assentfrom boys 7 and older before examina-tion. Data for each subject were collectedon a form with numbered drawings andverbal anchors to maximize accuracy.The physical examination includedheight and weight, using each clini-cian’s office equipment, Tanner staging,testicular volumemeasurement from 1through 4 mL, and breast palpation forgynecomastia. Testicular volume wascollected for each testis as a categori-cal variable: #1, 2, 3, or $4 mL.Examiners graded down the Tannerstage or testis volume if eitherappeared to fall between categories.Additional demographic data wereascertained by observation, question-ing, and medical chart review.

Data Analysis

We defined continuous age (years) asthe number of days between the monthof birth, (assuming the subject wasborn on the first of the month), and theexamination date divided by 365.25.When necessary, continuous age wascategorized as age rounded to thenearest year. We classified subjects asAfrican American if African Americanwas indicated on the study form (re-gardless of any other race/ethnicityindication), Hispanic if Hispanic eth-nicity was indicated (regardless of anyother indication other than AfricanAmerican), and white if only white wasindicated.

We calculated descriptive statistics,with exact binomial 95% confidenceintervals (CIs) for prevalence of Tannerstage2orgreaterpubichairandgenitaldevelopment within each age category.We used stratified Mantel-Haenszelrow mean score statistics to assess

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homogeneity of prevalences by race/ethnicity adjusted for age group.

Median ages and SDs for transition intoTanner stages 2 to 5 were estimated byusing probit regression, which linksa linear combination of covariates to thecumulative normal probability of havingachieved a stage. In probit analysis, themedian age is assumed to equal themean. For testicular volume analysis, weused the larger of the testes if there wasa right-left difference.8 Foreachoutcome,the probit model adjusted for continu-ous age, categorical race/ethnicity (ref-erence group: whites), and theirinteraction. Model coefficients wereused to jointly test (a = 0.05) forequality of the mean ages of transitionacross the 3 race/ethnicity groups.Pairwise comparisons of race/ethnicitygroups were conducted with Bonfer-roni correction for multiple testing (ie,significance level a = 0.05/3 = 0.017).We calculated 95% CIs for the meanages of transition using Fieller’s Theo-rem.13 All analyses used SAS 9.2 (SASInstitute, Inc, Cary, NC).

RESULTS

We enrolled 5355 participants from 144sites between 2005 and 2010. After ex-clusion for chronic conditions ormedications that could affect puberty,missing data, or “other racial” cate-gory, 4131 boys remained for analysis(Fig 1). Of these, 2070 (50%) wereclassified as white, 1062 (26%) AfricanAmerican, and 999 (24%) Hispanic.Demographic and clinical character-istics of the study population are pre-sented in Table 1.

Fig 2 shows the proportion of boys(95% CIs) entering Tanner stage 2 orgreater genital development and pubichair growth by race/ethnicity and age.Adjusted for age, the proportion forboth genital and pubic hair de-velopment was found to be statisticallydifferent among the 3 race/ethnicitygroups (P , .001). African American

boys had higher proportions at a givenage for both genital and pubic hairdevelopment than white (both P ,.001) and Hispanic boys (both P ,.001), but white and Hispanic boysshowed no difference (P = .54 and P =.16, respectively).

Table 2 presents estimates of the meanage of transition to stages 2 to 5 forgenital development and pubic hairgrowth. Entry into stage 2 genital de-velopment occurred at 10.14 years forwhite boys, 9.14 for African Americanboys, and 10.04 for Hispanic boys.

FIGURE 1Derivation of the SSCIB study population.

TABLE 1 Demographic and Clinical Characteristics of Study Subjects by Race/Ethnicity

Characteristic White African American Hispanic

n (%) n (%) n (%)

Payment statusMedicaid 349 (17.5) 673 (65.9) 607 (63.0)Insurance 1618 (80.9) 340 (33.3) 333 (34.6)Self-pay 32 (1.6) 9 (0.8) 23 (2.4)Total 1999 1022 963

Chronic diseaseNone 1691 (81.8) 775 (73.3) 806 (80.7)Asthma only 137 (6.6) 149 (14.1) 82 (8.2)Other only 217 (10.5) 115 (10.9) 101 (10.1)Asthma and other 22 (1.1) 18 (1.7) 10 (1.0)Total 2067 1057 999

Chronic disease and medicationsNone 1647 (79.8) 756 (71.7) 796 (79.9)Disease, no chronic medications 43 (2.1) 16 (1.5) 9 (0.9)Medication, no chronic diseases 196 (9.5) 151 (14.2) 119 (11.9)Chronic diseases and chronic medications 179 (8.6) 134 (12.6) 73 (7.3)Total 2065 1060 997

History of genital abnormalitiesNone 1961 (95.9) 1011 (96.8) 957 (97.9)Undescended testes 28 (1.4) 13 (1.3) 8 (0.8)Hypospadias 12 (0.6) 3 (0.3) 2 (0.2)Varicocele 16 (0.8) 3 (0.3) 4 (0.4)Undescended testes+hypospadias 3 (0.2) 1 (0.1) 0 (0)Other 26 (1.1) 12 (1.2) 7 (0.7)Total 2046 1043 978

There were 147 missing values for payment status, 8 missing for chronic disease, and 64 missing for history of genitalabnormalities.

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Overall, these were statistically different(P , .0001). Pairwise differences werefound between African American andwhite boys (P , .0001), African Ameri-can and Hispanic boys (P , .001), butnot between white and Hispanic boys(P = .48). For pubic hair, mean ages ofentry into stage 2 were 11.47, 10.25, and11.43 years respectively; overall, thesewere statistically different (P , .0001).Pairwise differences were found be-tween African American and white boys(P , .001), and African American andHispanic boys (P , .001), but not be-tween white and Hispanic boys (P = .69).

Because earlier pubertal studiesassessing testicular volume have usedvolumes of 3 mL, $3 mL, .3 mL, and$4 mL8,14–17 as indicative of centralpubertal take-off, we present meanages of transition for both $3 mL and$4 mL (Table 2). Data on Cincinnatiboys15 and Swedish boys16 show thatthe transition from 2 to 3 mL indicatespubertal take-off. White boys in thisstudy reached a mean age of transitionto 3 mL at 9.95 years, African Americanboys at 9.71, and Hispanic boys at 9.63,with no significant difference (P = .11).Mean ages for reaching volumes of$4mL were 11.46, 11.75, and 11.29 years,respectively. Overall, these were foundto be statistically different (P = .008),with pairwise significance only be-tween African American and Hispanicboys (P = .002).

Data on progression to full sexual ma-turity present a slightly different pat-tern. For stages 3 and 4, statisticaldifferences by race/ethnicity were ob-served, but not for stage 5. PairwisedifferencesbetweenwhiteandHispanicboys were found for stages 3 and 4pubic hair and stage 4 genital de-velopment. Estimated ages for entryintostage5 (sexualmaturity) forgenitaldevelopment were 15.57, 15.51, and15.58 years, and 15.83, 15.72, and 15.89for pubic hair for white, African Amer-ican, and Hispanic boys, respectively.

FIGURE 2Percentages (95% confidence intervals) of white non-Hispanic, African American non-Hispanic, andHispanic boys with secondary sexual characteristics at sexual maturity Stage 2 or greater.

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Table 3 shows the ages of onset ofsecondary sexual characteristics fromthe Marshall and Tanner study, earlierUS studies, and our own. In particular,SSCIB white and Hispanic boys enteredstage 2 genitalia 1.5 years earlier thanthe boys studied by Marshall and Tan-ner. African American boys are morethan 2 years earlier.

Because data are conflicting on theeffect of obesity on boys’ puberty,9,18–20

we examined relationships between

BMI and ages of onset of sexual matu-rity stages. Pooling race/ethnicity (be-cause of small sample size) andcontrolling for age, boys with BMI,15th percentile had later mean agesof transition to stages 2 to 4 for genitaland pubic hair growth than boys withBMI.85th percentile (data not shown).No other comparisons for stages or BMIcategorieswere significantly different. Itmust be noted that because pubertaldevelopment itself is associated with an

increase in BMI, and that existing BMIstandards for youth are based onchronologic age, our cross-sectionaldata limit the assessment of cause-and-effect relationships between BMIand pubertal timing.

DISCUSSION

We observed that onset of secondarysexual characteristics in US boys asseen in office practice appears to occurearlier than in previous US studies andthe 1969 British study commonly usedfor pubertal norms.1,11 In addition, wefound significant differences in the ageof onset of stage 2 genital and pubichair growth between African Americanboys as compared with white and His-panic boys and transition to testicularvolumes $4 mL (but not 3 mL). Themeaning of this finding is unclear, as noexisting studies inform differences inmean testicular size at given ages, byrace/ethnicity, and sexual maturitystage; or in racial/ethnic differences inthe rate of advancement through theTanner stages over time.

Of consequence are the differences wefound comparing our results with the40-year-old data from Marshall andTanner’s landmark study on 228 whiteinstitutionalized boys in London.11

White boys in our study entered stage 2genital growth 1.5 years earlier thanthe British boys (10.14 vs 11.60 years ofage). Comparing ages of onset of stage2 pubic hair growth from the Britishstudy (estimated at 13.4 years of age)is not possible because, as the authorsstated, the age “was not accuratelydetermined,” because assessmentswere from photographs.11 Their ob-servation for entry into stage 3 pubichair, 13.9 years, is likely more reliable,as stage 3 hair would be visible inphotographs. White SSCIB study sub-jects entered stage 3 pubic hair de-velopment at a mean of 12.89 years,a full year earlier. For stage 2 pubichair, US studies from 1948 to 1995

TABLE 2 Median (Mean) Ages of Transition for Secondary Sexual Characteristics and TesticularVolume Among White Non-Hispanic, African American Non-Hispanic, and Hispanic Boys

Median, y SD 95% CI P value of OverallRace/Ethnicity Differences

Genital development.Stage 2 ,.0001White 10.14 2.18 (9.97–10.31)African American 9.14 2.10 (8.88–9.39)Hispanic 10.04 1.83 (9.81–10.26)

Stage 3 ,.0001White 12.49 1.44 (12.36–12.61)African American 11.58 1.65 (11.38–11.77)Hispanic 12.31 1.18 (12.14–12.47)

Stage 4 ,.0001White 13.72 1.23 (13.61–13.83)African American 13.04 1.72 (12.85–13.23)Hispanic 13.45 1.37 (13.28–13.61)

Stage 5 .9368White 15.57 1.53 (15.42–15.73)African American 15.51 2.33 (15.21–15.87)Hispanic 15.58 1.64 (15.34–15.86)

Pubic hairStage 2 ,.0001White 11.47 1.62 (11.33–11.61)African American 10.25 1.79 (10.03–10.46)Hispanic 11.43 1.53 (11.23–11.62)

Stage 3 ,.0001White 12.89 1.18 (12.77–12.99)African American 11.79 1.56 (11.60–11.97)Hispanic 12.57 1.15 (12.41–12.73)

Stage 4 ,.0001White 13.76 1.23 (13.65–13.87)African American 13.06 1.67 (12.87–13.24)Hispanic 13.38 1.22 (13.22–13.54)

Stage 5 .6772White 15.83 1.49 (15.68–16.01)African American 15.72 1.97 (15.44–16.05)Hispanic 15.89 1.58 (15.64–16.22)

Testicular volume$3 mL .1109White 9.95 2.44 (9.76–10.13)African American 9.71 2.43 (9.43–9.96)Hispanic 9.63 2.39 (9.36–9.89)

$4 mL .0079White 11.46 1.97 (11.30–11.62)African American 11.75 1.83 (11.54–11.95)Hispanic 11.29 1.83 (11.07–11.50)

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TABLE3

Ages

ofPubertal

Events

inMales

inUS

andtheBritish

MarshallandTanner

Studies

Study/

Authors

Data

Collected,

Year

Span

Type of

Study

Country

Subjects

Age

Range,

y

MeanAge,y

TV$

3mL

TV$4mL

G 2G 3

G 4G 5

PH2

PH3

PH4

PH5

Marshall

and

Tanner

11

1950s–

1970s

Mixed

England

228White

$8

____

11.6White

12.9White

13.8White

14.9White

__13.9

14.4White

15.2White

Fels Institute

21

1930s–

1940s

LUnited

States

59White

9–21

____

11.5White

12.7White

13.4White

17.3White

12.2White

13.3

13.9White

16.1White

NHES

II/III22

1963–

1970

C-S

United

States

3047

White

12–17

____

“similartoMarshall&

Tanner,w

hiteand

AfricanAm

erican”

“similartoMarshall&

Tanner,w

hiteand

AfricanAm

erican”

LeeStudy38

1969–

1974

LUnited

States

36Not

clearly

specified

9–17

____

11.9White

13.2White

14.3White

15.1White

12.3White

13.9

14.7White

15.3White

Bogalusa

Heart

Study23

1973–

1974

C-S

United

States

1153

White;

676

African

American

5–14

____

11.8White;

11.2

African

American

____

__12.5White;

11.7

African

American

____

__

HHANES

241982–

1984

C-S

United

States

704Mexican

American

10–17

____

12.4Mexican

American

13.5 Mexican

American

14.6 Mexican

American

16.3Mexican

American

12.8Mexican

American

13.6Mexican

American

14.6Mexican

American

16.1Mexican

American

NHANES

III5

1988–

1994

—United

States

536White;

797

African

American;

781

Mexican

American

8–19

____

10.1White;

9.5African

American;

10.4

Mexican

American

12.4White;

11.8

African

American;

12.5

Mexican

American

13.5White;

13.4

African

American;

13.7

Mexican

American

15.9White;

14.9

African

American;

15.7

Mexican

American

12.0White;

11.2

African

American;

12.3

Mexican

American

12.6White;

12.5

African

American;

13.1

Mexican

American

13.5White;

13.7

African

American;

14.1

Mexican

American

15.7White;

15.4

African

American;

15.8

Mexican

American

Biro

Study15

1984–

1987

LUnited

States

278White;

237

African

American

10–18

12.18 White;

12.18

African

American

____

____

__12.8White/

African

American

13.7White/

African

American

14.6White/

African

American

15.2White/

African

American

Susm

anStudy25

2000–

2006

LUnited

States

364White;

63African

American

9.5– 15.5

____

10.4White;

9.6African

American

12.4White;

11.6

African

American

13.6White;

12.8

African

American

14.9White;

14.3

African

American

11.5White;

10.5

African

American

12.8White;

11.9

African

American

13.7White;

13.0

African

American

15.1White;

14.5African

American

SSCIB

2005–

2010

C-S

United

States

2070

White;

1062

African

American;

999

Hispanic

6–16

9.95

White;

9.71

African

American;

9.63

Hispanic

11.46 White;

11.75

African

American;

11.29

Hispanic

10.14White;

9.14

African

American;

10.04

Hispanic

12.49White;

11.58

African

American;

12.31

Hispanic

13.72White;

13.04

African

American;

13.45

Hispanic

15.57White;

15.51

African

American;

15.58

Hispanic

11.47White;

10.25

African

American;

11.43

Hispanic

12.89White;

11.79

African

American;

12.57

Hispanic

13.76White;

13.06

African

American;

13.38

Hispanic

15.83White;

15.72

African

American;

15.89

Hispanic

C-S,cross-sectional;G,genital;L,longitudinal;NH

ES,NationalH

ealth

Exam

inationSurvey;PH,pubichair;TV,testicular

volume.

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found a mean age of onset from 12.0 to12.8 years of age5–7,15,21–23 for whiteboys. Results from SSCIB boys demon-strate this is occurring 6 months toa year earlier than previously repor-ted.

Although comparisonof our resultswiththose of earlier studies is limited be-cause of lack of early data onminoritiesand differences in methodologies, so-cioeconomic status, age at enrollment,and small numbers of subjects in moststudies,1,4,18 the 6-month to 2-year ear-lier development of secondary sexualcharacteristics or testicular enlarge-ment as documented in our study isnotable. Few older studies on AfricanAmerican or Hispanic boys exist. Resultsfrom the 40-year-old nationally repre-sentative US Health Examination Survey,Cycle III, on African American boys werestated to be “comparable to the meanages in Marshall and Tanner’s data onwhite boys.”22 Foster et al,23 in a study 35years ago, found African American boysin Louisiana began genital and pubichair development at 11.2 and 11.7 yearsas compared with our ages of 9.14 and10.25.

The only previous US studies on His-panic boys involved Mexican Americanboys: the Hispanic Health and Exami-nation Survey (HHANES), 1982 to 1984,and NHANES III, 1988 to 1992.5–7,24 Be-cause we enrolled Hispanic boys with-out regard to country of origin, directcomparison may not be valid. HHANESand NHANES III found attainment of gen-ital stage 2 declined from 12.4 to 10.4years of age over a 10-year period, al-though the accuracy of the latter’s genitaldata has been questioned as discussedin the following paragraph.5–7,24 SSCIBHispanic boys entered stage 2 genitaldevelopment at 10.04 years.

Findings for genital data between thePROS study and NHANES III are similar;however, it should be noted that severalauthors have questioned the accuracyof the NHANES III results,5,8,9,18 which

found very early onset of genital stage2 for all groups and noted that the 2-year span between genital stage 2 andpubic hair stage 2 was longer than thatfound in any other puberty study. Thus,genital Tanner stage misclassificationmay have occurred and the genital datamay be unreliable. Stage 2 pubic haironset for Mexican American boys be-tween HHANES and NHANES III declinedfrom 12.8 to 12.3 years. SSCIB Hispanicboys reached stage 2 pubic hair ata mean of 11.43 years of age. Non-Hispanic white and African Americanboys in SSCIB reached stage 2 pubichair 0.53 and 0.95 years earlier thanthe NHANES III boys. Comparisons ofpubic hair stages should be more re-liable, as assessment of pubic hair isnot as subjective as that of genital de-velopment. Our findings are also simi-lar to a recent longitudinal pubertystudy that included 364 white and 63African American boys (Table 3).25

Very few European or US studies haveincluded testicular volumes. Largo andPrader’s landmark 198314 longitudinalstudy on white Swiss boys proposedtesticular volume of 3 mL as the mostaccurate sign of central pubertal take-off based on their earlier work, laterconfirmed by the Cincinnati15 andSwedish studies.16 Boys in the Swissstudy were a mean age of 11.2 at gen-ital stage 2 and 11.8 at a testicularvolume of 3 mL. The study by Biro et al15

is the only US puberty study thatreported testicular volumes. Theirsubjects, studied from 1984 to 1987(Frank M. Biro, MD, personal commu-nication, 2010), had a mean age of12.18 years when reaching a volume of3 mL, with no differences between thewhite and African American boys.SSCIB white and African American boyswere 2.23 and 2.47 years younger, re-spectively. Recent data from Denmarkalso report a decline in age forachieving a testicular volume .3 mL.8

Because our study is the first US study

to measure testicular volumes onwidely distributed boys, it can serve asa baseline for future studies.

We also note the pattern presented byour data on progression to stage 5genital development and pubic hairgrowth indicating sexual maturity. Oursubjects reached stage 5 at ages 15.7 to15.8 for all racial/ethnic groups, similarto the NHANES III data5; however, ourstage 5 probit model estimates (in-cluding comparisons of race/ethnicity)should be interpreted with cautionbecause they are artificially boundedby SSCIB’s maximum enrollment age of16 years. It is interesting that the 2010US longitudinal study found boys’ agefor genital maturity to be 14.9 and 14.3for white and African American boys,respectively.25

The strengths of the PROS study includeits large sample size and broad geo-graphical and minority patient repre-sentation. In addition, observationsweremade only onwell boys in primarycare sites by trained pediatricians andother clinicians. Testicular volumeswere measured through 4 mL.

The study has several limitations. Ourconvenience sample of US boys seen inpediatric offices for well-child care isnot a statistically representative sam-ple of the US population. The studyresults could be questioned if the boysin our study were biologically differentfrom boys in the US population; how-ever, there is no plausible reason thatwould support this contention. Becausethese data are cross-sectional, statis-tical methods allow for only the esti-mation of mean ages of transition intothe sexual maturity stages. Longitudi-nal data are required to assess du-ration, peak height velocity, andrelationships between duration andtiming of pubertal stages. Population-based longitudinal studies in theUnited States have not been conductedbecause of methodological challengesand expense. Our age calculations may

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lack precision because, to protect pri-vacy, we could not collect the day ofbirth. This, however, is unlikely to haveintroduced meaningful differences.Our training in sexual maturity stagingand orchidometer use was designedwith the input of several pediatricendocrinologists and accomplishedthrough an instruction manual withphotographs and explanatory and in-structive text. As previously described,testing ensured staging proficiencyamong qualifying clinicians. We areaware of no large US study that has socarefully documented its trainingmethods with a manual and testing,and shown interrater reliability amonga sample of those trained. Although itwould have been ideal to have assess-ments completed by pediatric endo-crinologists with extensive experiencein sexual maturity staging, this was notfeasible in a study of thousands ofnonreferred children across 41 states.Testicular volumes were assessed as#1, 2, 3, or $4 mL; therefore, datafrom studies that used .3 mL but ,4mL rather than $3 mL or $4 mL astheir criteria for central pubertal take-off are not strictly comparable. Ultra-sound, regarded as a more precisemethod for measuring testes,26,27 is notpractical for large-scale studies and isnot part of the usual pediatric exami-nation.28 Volume comparisons with thePrader orchidometer have been shownto be reasonably accurate.27

In conclusion, our data suggest that USboys are beginning genital and pubichair growth earlier than several deca-des ago in concordance with recentreports on girls.1 These data are con-sistent with recent trends from othercountries, such as Denmark, Sweden,Great Britain, Italy, and China.2,8,29–33

For example, urban Han Chinese boysachieve a testicular volume of $4 mL(13% by age 9) and spermarche earlierthan studies conducted several deca-des ago; Danish boys achieve a testic-

ular volume .3 mL more than 3months earlier now than 15 years ago.

Our findings are somewhat surprising,given that factors associated with ear-lier physical development in girls, suchas overweight and certain endocrinedisrupters,34 are not known to be as-sociated with earlier development inboys and could even be theorized tohave a delaying effect.2,35 Our data donot allow for an analysis of the possibleunderlying mechanisms of these ob-served decreases in the apparent age ofonset of secondary sexual character-istics as assessed by physical exami-nation. They do, however, demonstratethe importance in the physical exami-nation of boys of observing the ontogenyof changes in testicular volumes alongwith the stage of pubic hair growth. Forexample, in a 7-year-old, the presence ofpubic hair with concomitant testicularvolume increase needs close scrutinyand endocrinologic evaluation to besure that true sexual precocity is notoccurring. In the absence of increasedtesticular volume or systemic changesof androgenization, the more likelyprocess in this example would be that of“benign” premature adrenarche.

Current environmental factors, in-cludingexposure tochemicals, changesin diet, less physical activity, and othermodern lifestyle changes and expo-sures may be related to this apparentrapid decrease in the age of onset ofsecondary sexual characteristics andmay not reflect healthy conditions.36,37

Psychological, emotional, and behav-ioral affects of earlier sexual maturitymay be pivotal, given the current phe-nomena of social and emotional delayin achieving adulthood.4,33 Longitudinaltracking is needed to clarify any impactof overweight/obesity on boys’ sexualdevelopment. The secular decrease weobserved in ages of onset of secondarysexual characteristics in US boysrequires further study.

ACKNOWLEDGMENTSThe pediatric practices that partici-pated in this study are listed by Ameri-can Academy of Pediatrics chapter. Thelisting of participants’ names does notimply their endorsement of the dataand conclusions. Alabama: GreenvalePediatrics–Alabaster (Alabaster), Phy-sicians to Children (Montgomery), Uni-versity of Alabama at BirminghamSchool of Medicine, Huntsville Campus(Huntsville). Alaska: Anchorage Pediat-ric Group LLC (Anchorage). California-1:Palo Alto Medical Foundation (LosAltos), Palo Alto Medical Foundation(Palo Alto), Palo Alto Medical Founda-tion (Mountain View), Pediatric and Ad-olescent Medical Associates of thePacific Coast Inc (Salinas), Practice ofAnita Tolentino-Macaraeg MD (Hollister),Practice of Razia Sheikh MD (Fresno),Shasta Community Health Center(Redding); California-2: Boulevard Pedi-atrics Medical Group Inc (Encino),Children’s Health Center at MattelChildren’s Hospital University of Cali-fornia Los Angeles (Los Angeles), LomaLinda University Health Care (MorenoValley), University of California LosAngeles Manhattan Beach Pediatrics(Manhattan Beach), University of Cali-fornia Los Angeles West Los AngelesOffice (Los Angeles); California-3: Clini-cas de Salud del Pueblo, Calexico Clinic(Calexico); California-4: Edinger Medi-cal Group and Research Center Inc(Fountain Valley), Southern OrangeCounty Pediatric Associates (RanchoSanta Margarita). Colorado: Children’sClinic of Pueblo PC (Pueblo), DenverPediatrics (Thornton), Rocky MountainPediatrics PC (Lakewood), Rocky Moun-tain Youth Clinics (Thornton). Connect-icut: Mauks Koepke Medical LLC(Danbury). Delaware: Pediatric Associ-ates (Newark), Pediatric Practice Pro-gram Christiana Care Health System(Wilmington), East Military: Naval Med-ical Center–Portsmouth (Chesapeake).Florida: Altamonte Pediatric Associates

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(Altamonte Springs), Beaches FamilyHealth Center (Jacksonville), EastsideFamily Practice Center (Jacksonville),Family Health Center–East and OviedoChildren’s Health Center (Orlando),Orlando Regional Healthcare (Orlando),Practice of Joseph Scarano, MD (Bra-denton), Practice of Mirtha E. CuevasMD Inc (Orlando), Santa Rosa Pediatricsof Florida (Milton), WestConnect FamilyHealth Center (Jacksonville). Georgia:The Pediatric Center (Stone Mountain).Hawaii: Children’s Medical AssociationInc (Aiea), Island Youth Heart andHealth Center (Hilo), Practice of Chris-tine S. Hara MD (Honolulu), Practice ofJeffrey Lim MD Inc (Honolulu). Iowa:University of Iowa (Iowa City). Idaho:Saint Alphonsus Medical Group Pediat-rics (Caldwell). Illinois: Practice ofMary E. Lewis MD PC (La Grange), SWPediatrics (Orland Park). Indiana: Jef-fersonville Pediatrics (Jeffersonville),JMS Primary Care Center (Indianapo-lis). Kansas: Ashley Clinic (Chanute),University of Kansas School of Medicine(Wichita). Louisiana: Ochsner Children’sHealth Center (New Orleans). Massa-chusetts: Baystate Pediatric Associates(Springfield), Baystate Pediatric Group(Springfield), Burlington Pediatrics(Burlington), Holyoke Pediatric Associ-ates (Holyoke), Quabbins Pediatrics(Ware), University of MassachusettsMemorial Pediatrics and Internal Med-icine (Westburough), University of Mas-sachusetts Memorial Pediatric PrimaryCare (Worcester), Wareham PediatricsAssociates (Wareham), Worcester Pedi-atric Associates (Worcester). Maryland:Cambridge Pediatrics LLC (Waldorf),Potomac Pediatrics (Rockville), Practiceof Steven E. Caplan MD PA (Baltimore),Shady Side Medical Associates (ShadySide), Waldorf Pediatrics (Waldorf).Maine: Kennebec Pediatrics (Augusta),Maine Coast Memorial Hospital (Ells-worth). Michigan: Children’s Hospital ofMichigan (Detroit), DeVos Children’s Hos-pital (Grand Rapids), Hurley Children’sAttending Clinic (Flint), Southwestern

Medical Clinic (Stevensville). Minnesota:Brainerd Medical Center PA (Brainerd).Missouri: Priority Care Pediatrics LLC(Kansas City), Tenney Pediatric and Ad-olescent LLC (Kansas City). North Caro-lina: Carolinas Medical Center TeenHealth Connection (Charlotte), Golds-boro Pediatrics PA (Goldsboro). NorthDakota: Altru Clinic (Grand Forks).Nebraska: Children’s Physicians (Omaha).New Jersey: Delaware Valley PediatricAssociates PA (Lawrenceville). New Mex-ico: Ben Archer Health Center (Truth orConsequences), Presbyterian FamilyHealthcare–Rio Bravo (Albuquerque),University of New Mexico Hospital(Albuquerque). Nevada: Sparks Pediat-ric and Adolescent Medicine (Sparks).New York-1: Outer East Side HealthClinic (Buffalo), Saint Peters HealthCenter for Children (Albany); NewYork-2: Maimonides Infants and Child-ren’s Hospital (Brooklyn), Practice ofLuis O. Herrera MD PC (Freeport), Prac-tice of R. Karim MD & L. Ganesh MD(Rego Park), RidgewoodMedical andDen-tal (Brooklyn); New York-3: Bronx Leba-non Pediatric Clinic–Third Avenue(Bronx), Haverstraw Pediatrics LLP(Haverstraw), Montefiore Medical Cen-ter (Bronx), Pediatric Practice Bronx–Lebanon Hospital (Bronx), Practice ofJulissa Baez MD PC (Bronx), SoundShore Medical Center (New Rochelle),Union Community Health Center (Bronx).Ohio: Children’s Choice Pediatrics (Stow),Ohio Pediatrics (Kettering), PediatricAssociates of Lancaster (Lancaster),Professional Pediatrics Inc (Hilliard),The Cleveland Clinic Wooster (Woos-ter). Oklahoma: Northwest Pediatrics(Enid), Shawnee Medical Center Clinic(Shawnee). Oregon: OHSU DoernbecherPediatrics–Westside (Portland). Pennsyl-vania: Saint Chris Care at NortheastPediatrics (Philadelphia), Shaikh Pediat-rics PC (Tobyhanna). Quebec: CliniqueEnfant-Medic (Dollard des Ormeaux).Rhode Island: Northstar Pediatrics (Prov-idence), Practice of Marvin Wasser MD(Cranston). South Carolina: George-

town Pediatric Center PA (George-town), MUSC Pediatric Primary Care(Charleston). Texas: Building Blocks Pe-diatrics (Pleasanton), Child Care Asso-ciates (San Antonio), Laredo Pediatricsand Neonatology PA (Laredo), Practiceof Sarah L. Helfand MD (Dallas), TexasChildren’s Hospital (Houston), TexasTech Pediatric Clinic (Odessa), Winns-boro Pediatrics (Winnsboro). Utah:Practice of Joseph M. Johnson MD(Provo), Salt Lake Clinic (Sandy), Uni-versity of Utah Health Sciences Center(Salt Lake City), University South MainPublic Health Center (Salt Lake City),Utah Valley Pediatrics LC (AmericanFork). Virginia: Alexandria Lake RidgePediatrics (Alexandria), ChesapeakeMedical Group (Kilmarnock), EasternVirginia Medical School (Norfolk), River-side Pediatric Center (Newport News),Van Dorn Pediatrics and AdolescentMedicine (Alexandria). Vermont: Haganand Rinehart Pediatricians (South Bur-lington), University Pediatrics (Williston),University Pediatrics–UHC Campus (Bur-lington). Washington: Central Wash-ington Family Medicine (Yakima).Wisconsin: Beloit Clinic SC (Beloit), Co-lumbia–Saint Mary’s GermantownClinic (Germantown), Gundersen Lu-theran Medical Center (La Crosse),WaukeshaPediatric Associates (Waukesha).

National Medical Association PediatricResearch Network Practices (listedhere by state): Florida: Practice ofArlene E. HaywoodMD (Plantation). Ten-nessee:MeharryMedicalCollege (Nash-ville), PracticeofWillieMaeHubbardMD(Chattanooga).

Academic Pediatric Association’s Conti-nuity Research Network Practices(listed here by state): Florida: CarmenAlfaro, MD; University of South Florida(Tampa). Maryland: Maureen Parrott,MD; Susan Feigelman, MD; Universityof Maryland School of Medicine (Balti-more). Michigan: William Stratbucker,MD, MS; Devos Children’s Center (GrandRapids). New York: Daniel Neuspiel, MD;

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Beth Israel Medical Center (New York);Maureen Parrott, MD; Pamela Jacobs,MD; Lynn Garfunkel, MD; RochesterGeneral Pediatric Associates (Roches-ter). Ohio: Susan Monk, MD; MariaNanagas, MD; Dayton Children’s Medi-cal Center (Dayton). Texas: MichelleBarratt, MD, MPH; Kids Place, Universityof Texas (Houston).

We thank the following for their contri-butions to the study manual; Carlos J.Bourdony, MD, for his part in creating

the boys’manual; Marsha L. Davenport,MD, who provided photographs for theuse of the orchidometer; John Fuqua,MD, Marsha L. Davenport, MD, andAnita Azam, MD, who provided photo-graphs for certain aspects of Tannerstaging of boys; Stanley M. Coffman,Duke University Medical Center Medi-cal Illustrations, who provided draw-ings; and the University of NorthCarolina School of Medicine Depart-ment of Educational Media Services

for photography work. We also ac-knowledge Paul Kaplowitz, MD, ReubenRohn, MD, John Fuqua, MD, and SusanRose, MD, for their expert opinion onaspects of the study and their review ofthe manual. Finally, we thank The Gen-entech Center for Clinical Researchwho provided the initial orchidometersand Terry Brown, whose expert wood-working skills allowed for us to con-tinue providing orchidometers toclinicians.

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(Continued from first page)

www.pediatrics.org/cgi/doi/10.1542/peds.2011-3291

doi:10.1542/peds.2011-3291

Accepted for publication Jul 30, 2012

Address correspondence to Marcia E. Herman-Giddens, PA, DrPH, Department of Maternal and Child Health, Gillings School of Global Public Health, University ofNorth Carolina at Chapel Hill, 1450 Russell Chapel Road, Pittsboro, NC 27312. E-mail: mherman-giddens@unc.edu

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2012 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: Dr Reiter has received payment for services from NovoNordisk and Abbott. NovoNordisk produces growth hormone and Abbott producestestosterone. Neither of these agents were involved with this observational study. The small number of children receiving treatments with hormonal productswere excluded from analyses. The other authors have indicated they have no financial relationships relevant to this article to disclose.

FUNDING: Dr Herman-Giddens, Ms Steffes, Ms Harris, Dr Slora, and Dr Wasserman indicated that they have received some salary support from an unrestrictedresearch grant from Pfizer Inc. We are grateful for the support of the following funders: Pfizer Inc., The American Academy of Pediatrics, Genentech Center forClinical Research and Education, Health Resources and Services Administration, Maternal and Child Health Bureau, The Georgia Health Foundation, and The AAPResearch in Pediatric Practice Fund.

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