Timing of Puberty in Overweight Versus Obese Boys
BACKGROUND AND OBJECTIVE: Studies of the relationship of weight status with timing of puberty in boys have been mixed. This study examined whether overweight and obesity are associated with differences in the timing of puberty in US boys.
METHODS: We reanalyzed recent community-based pubertal data from the American Academy of Pediatrics’ Pediatric Research in Office Settings study in which trained clinicians assessed boys 6 to 16 years for height, weight, Tanner stages, testicular volume (TV), and other pubertal variables. We classified children based on BMI as normal weight, overweight, or obese and compared median age at a given Tanner stage or greater by weight class using probit and ordinal probit models and a Bayesian approach.
RESULTS: Half of boys (49.9%, n = 1931) were white, 25.8% (n = 1000) were African American, and 24.3% (n = 941) were Hispanic. For genital development in white and African American boys across a variety of Tanner stages, we found earlier puberty in overweight compared with normal weight boys, and later puberty in obese compared with overweight, but no significant differences for Hispanics. For TV (≥3 mL or ≥4 mL), our findings support earlier puberty for overweight compared with normal weight white boys.
CONCLUSIONS: In a large, racially diverse, community-based sample of US boys, we found evidence of earlier puberty for overweight compared with normal or obese, and later puberty for obese boys compared with normal and overweight boys. Additional studies are needed to understand the possible relationships among race/ethnicity, gender, BMI, and the timing of pubertal development.
- BPA —
- bisphenol A
- GD —
- genital development, PROS, Pediatric Research in Office Settings
- TV —
- testicular volume
What’s Known on This Subject:
Studies looking at the association between excess weight and timing of puberty in boys have produced mixed results, but these studies have often been limited by sample size and varying definitions of puberty.
What This Study Adds:
Data from a large community-based and diverse study of US boys suggest that the relationship between pubertal timing and body fat in boys may be nonlinear, with earlier puberty in overweight boys and later puberty in obese boys.
The association between body fat and timing of puberty is well established for girls, with the majority of studies reporting earlier attainment of puberty among overweight and obese girls.1–4 Fewer studies have been conducted in boys, and results from these studies have been mixed. Some studies have suggested that overweight and obese boys experience earlier attainment of puberty,5–7 similar to girls. In contrast, other studies have reported later attainment of puberty with excess weight.8–10
Existing studies on the relationship between weight and pubertal attainment in boys have been limited by small sample sizes,6,11,12 differing definitions of puberty (eg, using proxy measures of puberty such as timing of the pubertal growth spurt vs Tanner stage),7 and lack of multiple measures of puberty.8,13 Furthermore, most studies have not had adequate representation of minority populations to examine race and ethnicity differences in the timing of puberty.5–7 Therefore, we used the recent cross-sectional data from the large racially diverse study of puberty in boys by the American Academy of Pediatrics’ Pediatric Research in Office Settings (PROS) practice-based research network,12 one of the largest and most racially diverse studies to examine recent pubertal trends for boys in the US population, to examine whether overweight and obesity were associated with earlier or later attainment of puberty in US boys.
The methodology for the collection of data used in this study including clinician training and validation, data collection forms, population selection, and race/ethnicity designation have previously been described in detail.12,14 Clinicians were trained in Tanner staging for genital and pubic hair growth and use of a Prader orchidometer for measuring testicular volumes (TV) of 1 to 4 mL. A training manual was provided that contained photographs of sexual maturity stages from Tanner and van Wierengen, and providers had to pass a 2-part qualifying examination to clinically enroll patients. In a subset of practices, intraclass correlations were used to assess the degree to which rater pairs of practitioners were able to independently and reliably stage different measures of development. Two independent practitioners at each of 8 practices assessed development for 79 consecutive boys, with intraclass correlations of 0.94 for pubic hair, 0.83 for genital development (GD), and 0.61 for left and 0.69 for right testicular size.
Briefly, 212 trained clinicians from the PROS and Academic Pediatric Association’s Continuity Research Network (CORNET) recruited patients between July 2005 and February 2010. Boys ages 6 to 16 years being seen for well-child visits were eligible for enrollment. Clinicians recorded weight to the nearest 0.5 kg and height to the nearest cm using their own office measuring devices and techniques, Tanner stages, testicular volume measurement (coded as ≤1, 2, 3, or ≥4 mL), and results of breast palpation for gynecomastia. If Tanner stage or testis volume appeared to fall between categories, clinicians assumed the lower stage or volume, as this would provide a conservative estimate of timing of puberty and would ensure consistency across multiple clinicians. Race/ethnicity was classified by clinicians as African American (regardless of any other race/ethnicity indication), Hispanic if this ethnicity was indicated (regardless of any other indication other than African American), and white if only this category was indicated. Practice locations were 17% in the Midwest, 24% in the Northeast, 31% in the South, and 28% in the West.
For this analysis, we defined continuous age (years) as the number of days between the month of birth (assuming the subject was born on the first of the month), and the examination date divided by 365.25. Exact birthdate was not available due to internal review board restrictions. When necessary, continuous age was categorized as age rounded to the nearest year. Insurance status was used as a proxy for income.
Weight Status Categories
We used the Centers for Disease Control and Prevention growth percentiles to classify children into 3 categories: normal weight (BMI 5th to 84th percentile), overweight (BMI ≥85th and <95th percentile), and obese (BMI ≥95th percentile).15
Main Outcome Measures
The physical manifestations of childhood growth and development are the result of 2 separate but temporally related endocrinologic processes: puberty and adrenarche. Central puberty is regulated by the hypothalamic-pituitary-gonadal axis and is assessed by using testicular volume and genital development in boys.14,16 In contrast, adrenarche, which is assessed by using pubic hair development, is the result of maturational changes in the adrenal glands that trigger increased production of adrenal androgens.17,18 In this study, we were specifically interested in the relationship between obesity and central puberty; therefore, we used testicular volume and genital stages as our main outcome measures. We classified children as Tanner stage 2 genital development and greater versus Tanner stage 1; Tanner stage 3 genital development or greater versus Tanner stage 1 or 2; Tanner stage 4 genital development or greater versus Tanner stage 1, 2, or 3; and Tanner stage 5 genital development or greater versus Tanner stage 1, 2, 3, or 4. For testicular volume, we compared boys who had reached a testicular volume of ≥3 mL versus <3 mL, and ≥4 mL versus <4 mL, definitions that have been used in previous studies to define onset of puberty.12
We examined the distribution of puberty outcomes across the age spectrum, assessing the percentage of boys who reached Tanner stage GD2 or greater, GD3 or greater, GD4 or greater, and GD5 or greater, and testicular volume outcomes, overall and separately for weight status and by each race/ethnicity group. This permitted us to assess population distributions before conducting our probit models. We conducted probit regression models for each of the Tanner GD2 or greater, GD3 or greater, or GD4 or greater, and testicular volume to predict the probability of having puberty by age for each of the foregoing outcomes. For Tanner GD5 or greater, because no data were available after age 16, we used an ordinal probit regression model, which borrows strength from the other genital stages, to improve the estimates on the right tail (age 17+). All models were fitted by using a Bayesian approach via Proc MCMC in SAS. Following the Bayesian framework, we calculated median age and the corresponding 95% confidence intervals (CIs) for children of different weight groups using Monte Carlo simulations. We assumed statistical significance at a P value of <.05 and did not perform adjustment for multiple comparisons, as has been recommended in the statistical literature.19–21
In our initial analyses, we compared median age at a given Tanner stage for obese boys with all other boys and found no differences in median age at pubertal stage by testicular volume. However, we did find evidence of later onset of puberty for obese boys, which was primarily driven by associations in African American boys. Therefore, we elected to conduct a stratified analysis for each of the race/ethnicity groups, comparing median age at a given Tanner stage for normal weight versus overweight, normal weight versus obese, overweight versus obese, and normal weight versus overweight and obese boys. We report the results from these stratified analyses.
Figure 1 shows the exclusion criteria for this study. Boys were excluded from the sample for diseases or developmental conditions that could affect puberty (n = 75) or if they were taking oral or inhaled glucocorticoids (n = 313), stimulant medications (n = 476), or human growth hormone (n = 10). We also excluded an additional 52 boys for whom genital stage information was missing and 207 boys who had a missing BMI (n = 108) or who were underweight (<fifth percentile; n = 99). Because we wished to compare boys with excess weight with boys who were normal weight, we excluded underweight children from the analysis because studies have shown that underweight is associated with delayed puberty and could bias the results.22,23 When we compared boys in our sample with those who were excluded, there were no differences by age (P = .36) or race/ethnicity (P = .50).
Table 1 displays the demographic and clinical characteristics of boys in our sample. Half of boys (49.9%, n = 1931) were white, 25.8% (n = 1000) were African American, and 24.3% (n = 941) were Hispanic. Although there were no significant differences by age across racial groups, there were significant differences in weight status, insurance status, and pubertal status. A higher proportion of African American (26%) and Hispanic boys (28.9%) were obese compared with white boys (18.3%). These estimates were higher compared with recently reported national obesity prevalence data: 19.9% for black, 24.1% for Hispanic, and 12.6% for white boys.24 African American and Hispanic boys were also more likely to be enrolled in Medicaid than white boys. The table also shows median age at Tanner GD2 or greater through GD5 or greater for white, African American, and Hispanic boys.
Figure 2 shows median age at Tanner GD2 or greater through 5 or greater for white, African American, and Hispanic boys according to weight status. In analyzing the data for the entire study population, we did not find consistent associations across all stages, but there was evidence of a trend for earlier puberty in overweight compared with normal weight white boys for GD2 or greater (9.3 years [overweight] vs 10.0 years [normal weight]; P = .008) and GD5 or greater (14.5 years [overweight] vs 15.2 years [normal weight]; P = .001), and evidence for later puberty in obese compared with overweight and normal weight boys for GD5 or greater (15.4 years [obese] vs 14.5 years [overweight] and 15.2 years [normal weight]; P = .001).
For African American boys, we found evidence of a trend for later puberty for obese compared with overweight boys for GD3 or greater (11.7 years [obese] vs 10.6 years [overweight]; P = .0005) and GD4 or greater (13.2 years [obese] vs and 12.2 years [overweight]; P = .002), and for obese compared with normal weight boys for GD4 or greater (13.2 years [obese] vs 12.6 years [normal weight]; P = .006).
For Hispanic boys, we did not find significant differences in timing of puberty among weight status groups (Fig 2).
Figure 3 shows differences in median age at TV ≥3 mL or ≥4 mL for white, African American, and Hispanic boys, respectively. We found evidence for earlier puberty for overweight compared with normal weight boys for white boys but not for African American or Hispanic boys.
In a large, racially and ethnically diverse, community-based sample of US boys, we found evidence of earlier puberty for overweight compared with normal or obese boys, and evidence of later puberty for obese compared with normal and overweight boys. These differences were not consistent across all pubertal stages or all races/ethnicities. This apparent inconsistency provides insights into why the results of published analyses on the relationship between weight status and boys' puberty have been mixed.
Our findings of later puberty for obese boys and earlier puberty for overweight differ from previous studies, none of which have explored comparisons of pubertal timing across 3 weight groups. Wang conducted an analysis of puberty and weight using cross-sectional data from the NHANES and estimated a median age for Tanner genitalia stage for the overall cohort of boys aged 8 to 14 years.8 Boys were categorized as “early maturers” if they reached their Tanner genitalia stage earlier than the median age for that stage within the cohort; otherwise they were categorized as “late maturers.” Wang did not separate overweight from obese boys, grouping boys into 1 overweight or obese category (≥85th percentile). Interestingly, both groups were more likely to be classified as “late maturers.” However, that study did not examine overweight boys alone and did not examine race/ethnicity interactions for the association.
It is difficult to compare our data with other studies given that most studies have not distinguished between an overweight weight category exclusively or an obese category exclusively or they used BMI as a continuous variable. For example, a number of studies supported a negative association between timing of puberty and excess weight. Crocker et al reported a negative association between BMI z score and TV.10 Average TV was 7.5 mL (95% CI 6.9–8.1) for obese (n = 208) boys (mean age 11.7 years) compared with 9.2 mL (95% CI 8.6–9.8) for nonobese boys (mean age 11.2 years; n = 231), but this study did not perform comparisons of only overweight children. In a longitudinal cohort of mostly Caucasian boys from the National Institute of Child Health and Human Development Study of Early Childcare, Lee et al found that boys with the highest trajectory of BMI z score had the lowest attainment of Tanner stage 2 puberty by age 9 years, but this study did not compare children based on weight classification.9 Biro et al found that boys who had a higher fat mass as measured by sum of skinfolds had less advanced sexual maturation by age 12, and that boys who had a higher BMI and higher adiposity reached any maturation stage at older ages.25 Similar findings were reported from a Spanish male cohort.11
Studies in boys have also suggested the opposite association, with an earlier onset of puberty related to obesity. DeLeonibus prospectively followed a group of 44 obese Caucasian boys and 27 normal weight boys in Italy and reported that mean age at the onset of puberty was lower for the obese group (11.66 ± 1.00 years) compared with the nonobese group (12.12 ± 0.91 years).6 Ribeiro also reported similar findings in a population of 382 boys from Portugal.26 Much larger male cohort studies from England7 and Sweden27,28 that used age at peak height velocity as a proxy for the timing of pubertal maturation have also suggested that boys with a higher prepubertal BMI experience an earlier onset of puberty, although these studies consisted of men born in England between 1927 and 1956,7 and Swedish boys27,28 from the early 1970s, cohorts that grew up well before the onset of the worldwide childhood obesity epidemic.
It has been hypothesized that aromatase activity from adipose tissue may lead to excess estrogen production in boys, leading to possible delays in puberty29–31; therefore one might expect a linear association between fat mass and timing of puberty. However, given the earlier onset of puberty we found for overweight boys, and the later onset of puberty for obese boys, we speculate that it is possible that greater estrogen production in the obese boys could be suppressing the pubertal process for obese, but not overweight, boys.
Strengths of our study include the fact that the PROS subjects came from a community-based, large and diverse population of boys, which provided us with the opportunity to look at associations across 3 racial/ethnic groups. We also had access to dual measures of puberty, including both genital development and the gold standard measure for central puberty (TV),32 with interrater reliability for both Tanner staging and TV measurement demonstrated for examiners.14 Because of the large sample size, we were able to compare different and distinct weight categories.
Limitations of this study include several factors. First, the data were from a cross-sectional convenience sample of US boys seen in pediatric offices for well-child care. Because of the size and geographic diversity of the sample, children were assessed by nonendocrinologist pediatricians trained in pubertal assessment rather than by pediatric endocrinologists with more extensive experience in sexual maturity staging. Second, because of the large number of clinical centers participating, height and weight equipment were not calibrated. Third, BMI is a surrogate measure of adiposity, and studies have found that the relationship between body fat and BMI may vary depending on gender and race, as well as overall percent body fat.33 Fourth, to protect privacy, we could not collect the precise day of birth, although this is unlikely to have introduced meaningful differences in our results. There is great concern about the effects of endocrine disrupting compounds, including chemicals such as bisphenol A (BPA), polychlorinated biphenyl, and phthalates, on pubertal timing in boys.34 Given that BPA binds to estrogen receptors, there is concern that BPA exposure may lead to earlier onset of puberty in girls,35 but the effects are unknown for boys.
Our findings represent a unique contribution to our understanding of the complex relationship between boys’ puberty, overweight, and obesity. The relationship between pubertal timing and body fat in boys may be nonlinear, prompting the need for further clinical and mechanistic studies to evaluate pubertal outcomes and hormone levels across a spectrum of weight categories.
We are grateful for the following funders, which allowed this study to be completed: Pfizer Inc., The American Academy of Pediatrics, Genentech Center for Clinical Research and Education, Health Resources and Services Administration Maternal and Child Health Bureau, the Georgia Health Foundation, and the American Academy of Pediatrics Research in Pediatric Practice Fund. Finally, we thank the Genentech Center for Clinical Research, which provided the initial orchidometers, and Terry Brown, whose expert wood-working skills allowed for us to continue providing orchidometers to clinicians.
In addition, we thank the following people for their contributions to the study manual: Carlos J. Bourdony, MD, for his part in creating the boys' manual; Marsha L. Davenport, MD, who provided photographs for the use of the orchidometer; John Fuqua, MD, Marsha L. Davenport, MD, and Anita Azam, MD, who provided photographs for certain aspects of Tanner staging of boys; Stanley M. Coffman, Duke University Medical Center Medical Illustrations, who provided drawings; and the University of North Carolina School of Medicine Department of Educational Media Services for photography work. We also acknowledge Paul Kaplowitz, MD, Reuben Rohn, MD, John Fuqua, MD, and Susan Rose, MD, for their expert opinions on aspects of the study and their review of the manual.
Dr Lee had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Participating Practices: The pediatric practices that participated in this study are listed by American Academy of Pediatrics Chapter. The listing of participants’ names does not imply their endorsement of the data and conclusions. Alabama: Greenvale Pediatrics-Alabaster (Alabaster), Physicians to Children (Montgomery), University of Alabama School of Medicine-Huntsville Campus (Huntsville); Alaska: Anchorage Pediatric Group LLC (Anchorage), California-1: Palo Alto Medical Foundation (Los Altos), Palo Alto Medical Foundation (Palo Alto), Palo Alto Medical Foundation (Mountain View), Pediatric and Adolescent Medical Associates of the Pacific Coast Inc (Salinas), Practice of Anita Tolentino-Macaraeg, MD (Hollister), Practice of Razia Sheikh, MD (Fresno), Shasta Community Health Center (Redding); California-2: Boulevard Pediatrics Medical Group Inc. (Encino), Children’s Health Center at Mattel Children’s Hospital University of California-Los Angeles (UCLA; Los Angeles), Loma Linda University Health Care (Moreno Valley), UCLA Manhattan Beach Pediatrics (Manhattan Beach), UCLA West Los Angeles Office (Los Angeles); California-3: Clinicas de Salud del Pueblo, Calexico Clinic (Calexico), California-4: Edinger Medical Group and Research Center Inc. (Fountain Valley), Southern Orange County Pediatric Associates (Rancho Santa Margarita); Colorado: Children’s Clinic of Pueblo PC (Pueblo), Denver Pediatrics (Thornton), Rocky Mountain Pediatrics PC (Lakewood), Rocky Mountain Youth Clinics (Thornton); Connecticut: Mauks Koepke Medical LLC (Danbury); Delaware: Pediatric Associates (Newark), Pediatric Practice Program Christiana Care Health System (Wilmington); East Military: Naval Medical Center-Portsmouth (Chesapeake); Florida: Altamonte Pediatric Associates (Altamonte Springs), Beaches Family Health Center (Jacksonville), Eastside Family Practice Center (Jacksonville), Family Health Center-East and Oviedo Children’s Health Center (Orlando), Orlando Regional Healthcare (Orlando), Practice of Joseph Scarano, MD (Bradenton), Practice of Mirtha E. Cuevas, MD, Inc. (Orlando), Santa Rosa Pediatrics of Florida (Milton), WestConnect Family Health Center (Jacksonville); Georgia: The Pediatric Center (Stone Mountain), Hawaii: Children’s Medical Association Inc. (Aiea), Island Youth Heart and Health Center (Hilo), Practice of Christine S. Hara, MD (Honolulu), Practice of Jeffrey Lim, MD, Inc. (Honolulu); Iowa: University of Iowa (Iowa City); Idaho: Saint Alphonsus Medical Group Pediatrics (Caldwell); Illinois: Practice of Mary E. Lewis, MD, PC (La Grange), SW Pediatrics (Orland Park); Indiana: Jeffersonville Pediatrics (Jeffersonville), JMS Primary Care Center (Indianapolis); Kansas: Ashley Clinic (Chanute), University of Kansas School of Medicine (Wichita); Louisiana: Ochsner Children’s Health Center (New Orleans); Massachusetts: Baystate Pediatric Associates (Springfield), Baystate Pediatric Group (Springfield), Burlington Pediatrics (Burlington), Holyoke Pediatric Associates (Holyoke), Quabbins Pediatrics (Ware), University of Massachusetts Memorial Pediatrics and Internal Medicine (Westburough), University of Massachusetts Memorial Pediatric Primary Care (Worcester), Wareham Pediatrics Associates (Wareham), Worcester Pediatric Associates (Worcester); Maryland: Cambridge Pediatrics LLC (Waldorf), Potomac Pediatrics (Rockville), Practice of Steven E. Caplan, MD, PA (Baltimore), Shady Side Medical Associates (Shady Side), Waldorf Pediatrics (Waldorf); Maine: Kennebec Pediatrics (Augusta), Maine Coast Memorial Hospital (Ellsworth); Michigan: Children’s Hospital of Michigan (Detroit), DeVos Children’s Hospital (Grand Rapids), Hurley Children’s Attending Clinic (Flint), Southwestern Medical Clinic (Stevensville); Minnesota: Brainerd Medical Center PA (Brainerd); Missouri: Priority Care Pediatrics LLC (Kansas City), Tenney Pediatric and Adolescent LLC (Kansas City); North Carolina: Carolinas Medical Center Teen Health Connection (Charlotte), Goldsboro Pediatrics PA (Goldsboro); North Dakota: Altru Clinic (Grand Forks); Nebraska: Children’s Physicians (Omaha); New Jersey: Delaware Valley Pediatric Associates PA (Lawrenceville); New Mexico: Ben Archer Health Center (Truth or Consequences), Presbyterian Family Healthcare-Rio Bravo (Albuquerque), University of New Mexico Hospital (Albuquerque); Nevada: Sparks Pediatric and Adolescent Medicine (Sparks); New York-1: Outer East Side Health Clinic (Buffalo), Saint Peter's Health Center for Children (Albany); New York-2: Maimonides Infants and Children’s Hospital (Brooklyn), Practice of Luis O. Herrera, MD, PC (Freeport), Practice of R. Karim, MD and L. Ganesh, MD (Rego Park), Ridgewood Medical and Dental (Brooklyn); New York-3: Bronx-Lebanon Pediatric Clinic-Third Avenue (Bronx), Haverstraw Pediatrics LLP (Haverstraw), Montefiore Medical Center (Bronx), Pediatric Practice Bronx-Lebanon Hospital (Bronx), Practice of Julissa Baez, MD, PC (Bronx), Sound Shore Medical Center (New Rochelle), Union Community Health Center (Bronx); Ohio: Children’s Choice Pediatrics (Stow), Ohio Pediatrics (Kettering), Pediatric Associates of Lancaster (Lancaster), Professional Pediatrics Inc. (Hilliard), The Cleveland Clinic Wooster (Wooster); Oklahoma: Northwest Pediatrics (Enid), Shawnee Medical Center Clinic (Shawnee); Oregon: Oregon Health & Science University Doernbecher Pediatrics-Westside (Portland); Pennsylvania: Saint Chris Care at Northeast Pediatrics (Philadelphia), Shaikh Pediatrics PC (Tobyhanna); Quebec, Canada: Clinique Enfant-Medic (Dollard des Ormeaux); Rhode Island: Northstar Pediatrics (Providence), Practice of Marvin Wasser, MD (Cranston); South Carolina: Georgetown Pediatric Center PA (Georgetown), Medical University of South Carolina Pediatric Primary Care (Charleston); Texas: Building Blocks Pediatrics (Pleasanton), Child Care Associates (San Antonio), Laredo Pediatrics and Neonatology PA (Laredo), Practice of Sarah L. Helfand, MD (Dallas), Texas Children’s Hospital (Houston), Texas Tech Pediatric Clinic (Odessa), Winnsboro Pediatrics (Winnsboro); Utah: Practice of Joseph M. Johnson, MD (Provo), Salt Lake Clinic (Sandy), University of Utah Health Sciences Center (Salt Lake City), University South Main Public Health Center (Salt Lake City), Utah Valley Pediatrics LC (American Fork); Virginia: Alexandria Lake Ridge Pediatrics (Alexandria), Chesapeake Medical Group (Kilmarnock), Eastern Virginia Medical School (Norfolk), Riverside Pediatric Center (Newport News), Van Dorn Pediatrics and Adolescent Medicine (Alexandria); Vermont: Hagan and Rinehart Pediatricians (South Burlington), University Pediatrics (Williston), University Pediatrics-UHC Campus (Burlington); Washington: Central Washington Family Medicine (Yakima); Wisconsin: Beloit Clinic SC (Beloit), Columbia-Saint Mary’s Germantown Clinic (Germantown), Gundersen Lutheran Medical Center (La Crosse), Waukesha Pediatric Associates (Waukesha).
National Medical Association Pediatric Research Network Practices (listed here by state): Florida: Practice of Arlene E. Haywood, MD (Plantation); Tennessee: Meharry Medical College (Nashville), Practice of Willie Mae Hubbard, MD (Chattanooga).
Academic Pediatric Association’s Continuity Research Network Practices (listed here by state): Florida: Carmen Alfaro, MD, University of South Florida (Tampa); Maryland: Maureen Parrott, MD, Susan Feigelman, MD, University of Maryland School of Medicine (Baltimore); Michigan: William Stratbucker, MD, MS, DeVos Children’s Center (Grand Rapids); New York: Daniel Neuspiel, MD, Beth Israel Medical Center (New York), Maureen Parrott, MD, Pamela Jacobs, MD, Lynn Garfunkel, MD, Rochester General Pediatric Associates (Rochester); Ohio: Susan Monk, MD, Maria Nanagas, MD, Dayton Children’s Medical Center (Dayton); Texas: Michelle Barratt, MD, MPH, Kids Place, University of Texas (Houston).
- Accepted October 27, 2015.
- Address correspondence to Joyce M. Lee, MD, MPH, 300 NIB, Room 6E14, Campus Box 5456, Ann Arbor, MI 48109-5456. E-mail:
This study was presented in abstract form at the Pediatric Academic Societies Meeting in 2013.
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
FUNDING: Supported by Pfizer Inc., the American Academy of Pediatrics, Genentech Center for Clinical Research and Education, Health Resources and Services Administration Maternal and Child Health Bureau grant UA6MC15585, the Georgia Health Foundation, and the American Academy of Pediatrics Research in Pediatric Practice Fund.
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.
- Kaplowitz PB,
- Slora EJ,
- Wasserman RC,
- Pedlow SE,
- Herman-Giddens ME
- Davison KK,
- Susman EJ,
- Birch LL
- Sandhu J,
- Ben-Shlomo Y,
- Cole TJ,
- Holly J,
- Davey Smith G
- Wang Y
- ↵NHANES 1999–2000 public data release file documentation. Available at: http://www.cdc.gov/nchs/about/major/nhanes/nhanes99_00.htm. Accessed February 2, 2006
- Perneger TV
- Kulin HE,
- Bwibo N,
- Mutie D,
- Santner SJ
- Rogol AD,
- Clark PA,
- Roemmich JN
- Silventoinen K,
- Haukka J,
- Dunkel L,
- Tynelius P,
- Rasmussen F
- Daniels SR,
- Khoury PR,
- Morrison JA
- Zawatski W,
- Lee MM
- Copyright © 2016 by the American Academy of Pediatrics