Exposure to Per- and Polyfluoroalkyl Substances and Timing of Puberty in Norwegian Boys: Data from the Bergen Growth Study 2

Abstract

Per- and polyfluoroalkyl substances (PFAS) are widespread environmental contaminants with endocrine-disruptive properties. Their impact on puberty in boys is unclear. In this cross-sectional study, we investigated the association between PFAS exposure and pubertal timing in 300 Norwegian boys (9-16 years), enrolled in the Bergen Growth Study 2 during 2016. We measured 19 PFAS in serum samples and used objective pubertal markers, including ultrasound-measured testicular volume (USTV), Tanner staging of pubic hair development, and serum levels of testosterone, luteinizing hormone, and follicle-stimulating hormone. In addition to logistic regression of single pollutants and the sum of PFAS, Bayesian and elastic net regression were used to estimate the contribution of the individual PFAS. Higher levels of the sum of perfluorooctanesulfonic acid (PFOS), perfluorooctanoic acid (PFOA), perfluorononanoic acid (PFNA), and perfluorohexanesulfonic acid (PFHxS) were associated with later pubertal onset according to USTV (age-adjusted odds ratio (AOR): 2.20, 95% confidence interval (CI): 1.29, 3.93) and testosterone level (AOR: 2.35, 95% CI: 1.34, 4.36). Bayesian modeling showed that higher levels of PFNA and PFHxS were associated with later pubertal onset by USTV, while higher levels of PFNA and perfluoroundecanoic acid (PFUnDA) were associated with later pubertal onset by testosterone level. Our findings indicate that certain PFAS were associated with delay in male pubertal onset.

Keywords: adolescent; child; endocrine disruption; environmental health; puberty.

Figure 1

Flowchart of boys included in current study BGS2 = Bergen Growth Study 2. *To avoid inclusion of strictly prepubertal boys. **Due to missing data, certain individuals were excluded from specific analyses: Ultrasound-measured testicular volume (n = 6), Tanner pubic hair stage (n = 7), hormones (n = 7).

Figure 2

Proportion of boys having attained a pubertal testicular volume in each ∑4PFAS tertile group in boys aged 9–14.5 years in the Bergen Growth Study 2 (2016, Norway) (n = 228) USTV ≥ 2.7 mL = ultrasound-measured pubertal testicular volume of ≥2.7 mL. A generalized linear model was used to estimate the cumulative distribution curve in each tertile group of the sum of PFOS, PFOA, PFNA and PFHxS (∑4PFAS). The mean ages of reaching a pubertal testicular volume in the lowest, middle, and highest tertile were calculated as 11.26, 11.70, and 12.14 years.

Figure 3

Associations between PFAS serum concentrations and being prepubertal based on ultrasound-measured testicular volume (USTV) (n = 224) and serum testosterone level (n = 226) in boys aged 9–14.5 years in the Bergen Growth Study 2 (2016, Norway) LR = Logistic Regression. Log odds (with 95% confidence intervals/credible intervals) represent the log odds of being prepubertal and are adjusted for age in all analyses, and for the other PFAS in the Bayesian logistic regression analysis and elastic net analysis. PFOS, PFOA, PFNA, PFHxS, PFDA and PFUnDA were standardized using robust scaling with interquartile range. PFHpS and PFHpA concentrations were categorized as either below or above the quantification limit of 0.05 ng/mL.