Prenatal Environmental Exposure to Persistent Organic Pollutants and Reproductive Hormone Profile and Pubertal Development in Dutch Adolescents
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cohort and Study Design
2.2. Measurement of Prenatal POP Levels
2.3. Biochemical Analyses of Reproductive Hormones
2.4. Outcome Measures on Pubertal Development
2.5. Statistical Analyses of Data
3. Results
3.1. Study Group
3.2. Prenatal POP Levels
3.3. Levels of Reproductive Hormones
3.4. Pubertal Characteristics
3.5. Confounding Factors
3.6. PCBs and Pubertal Development in Boys
3.7. PCBs and Pubertal Development in Girls
3.8. OH-PCBs and Other POPs and Pubertal Development
4. Discussion
4.1. Prenatal PCB Exposure and Higher Testosterone Levels in Boys
4.2. Prenatal PCB Exposure and Larger Testicular Volume and Higher Pubic Hair Stage in Boys
4.3. Prenatal PCB Exposure and Higher FSH in Girls
4.4. Prenatal PCB Exposure and Higher Breast Stage in Girls
4.5. Prenatal OH-PCB Exposure and Pubertal Development
4.6. Different Findings Cohorts
4.7. Possible Mechanism
4.8. Strengths and Limitations
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Characteristic | Value | ||||
---|---|---|---|---|---|
Sex, boy/girl | 55/46 (54.5/45.5%) | ||||
Gestational age at birth (weeks) | 40 (37–42) | ||||
Age at examination (years) -Total cohort | 14.4 ± 0.8 | ||||
-RENCO cohort (n = 54) | 15.1 ± 0.4 | ||||
-GIC cohort (n = 47) | 13.6 ± 0.3 | ||||
Body mass index at examination | 20.0 ± 3.6 | ||||
Assessment Tanner stage by clinician [yes/no] (n = 97) | 33/64 (34/66%) | ||||
Maternal education level | |||||
Below average (≤11 years education) | 9 | ||||
Average (12–13 years education) | 41 | ||||
Above average (≥14 years education) | 51 | ||||
Maternal smoking during pregnancy [yes/no] | 13/88 (13/87%) | ||||
Maternal alcohol consumption during pregnancy [yes/no] | 21/80 (21/79%) | ||||
Maternal age at menarche (n = 97; years) Paternal timing growth spurt (n = 75) [early–average/late] | 12.8 ± 1.5 47/28 (63/37%) | ||||
Assessment of pubertal stage | |||||
Boys: -Testicular volume (n = 54; mL) | 10.0 ± 3.8 | ||||
Stage | 1 | 2 | 3 | 4 | 5 |
-Tanner genital stage (n = 53) | 2 | 14 | 22 | 14 | 1 |
-Tanner pubic hair stage (n = 53) | 4 | 8 | 15 | 23 | 3 |
Girls: -Tanner breast stage (n = 42) | 0 | 0 | 15 | 17 | 10 |
-Tanner pubic hair stage (n = 41) | 0 | 0 | 17 | 21 | 3 |
Questionnaire on pubertal development | |||||
Boys: -‘Did you observe growth of pubic hair?’ [yes] -‘If yes: from which age?’ (years) | 49 (89%) | 12.4 ± 0.92 | |||
-‘Did you notice that you have grown a lot in short time?(growth spurt)’ [yes] -‘If yes: from which age?’ (years) | 44 (80%) | 12.4 ± 1.10 | |||
-‘Have you had ejaculations?’ [yes] -‘If yes: from which age?’ (years) | 29 (53%) | 13.0 ± 0.69 | |||
-‘Did you notice voice break (lower voice)’ [yes] -‘If yes: from which age?’ (years) | 35 (64%) | 13.2 ± 0.76 | |||
Girls: -‘Did you observe breast growth?’ [yes] -‘If yes: from which age?’ (years) | 46 (100%) | 11.7 ± 1.20 | |||
-‘Did you notice that you have grown a lot in short time?(growth spurt)’ [yes] -‘If yes: from which age?’ (years) | 37 (80%) | 11.7 ± 1.37 | |||
-‘Did you observe growth of pubic hair?’ [yes] -‘If yes: from which age?’ (years) | 46 (100%) | 12.0 ± 1.06 | |||
-‘Have you had a period?’ [yes] -‘If yes: from which age?’ (years) | 39 (85%) | 12.4 ± 1.16 |
Boys | Girls | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Compound | Cohort | n | Mean | SD | SEM | t | p-Value | n | Mean | SD | SEM | t | p-Value |
PCB-153 a | RENCO | 26 | 93.19 | 41.00 | 8.04 | 2.77 | 0.008 | 28 | 110.53 | 40.11 | 7.58 | 4.67 | <0.001 |
COMPARE | 29 | 63.90 | 37.35 | 6.94 | 18 | 65.77 | 24.84 | 5.85 | |||||
OH-PCB-107 b | RENCO | 26 | 74.73 | 34.72 | 6.81 | 6.31 | <0.001 | 26 | 83.08 | 60.04 | 11.78 | 3.98 | <0.001 |
COMPARE | 28 | 27.59 | 16.29 | 3.08 | 17 | 31.94 | 21.29 | 5.16 | |||||
OH-PCB-146 b | RENCO | 26 | 82.42 | 34.71 | 6.81 | −1.22 | 0.227 | 26 | 84.85 | 42.75 | 8.38 | −2.57 | 0.016 |
COMPARE | 29 | 95.23 | 42.03 | 7.81 | 18 | 130.69 | 66.81 | 15.75 | |||||
OH-PCB-187 b | RENCO | 26 | 137.38 | 44.58 | 8.74 | 6.54 | <0.001 | 26 | 149.85 | 58.36 | 11.44 | 3.37 | 0.002 |
COMPARE | 29 | 73.94 | 22.64 | 4.20 | 18 | 96.95 | 38.17 | 9.00 |
Boys | Girls a | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Hormone | n | Mean | SEM | Median | Min | Max | n | Mean | SEM | Median | Min | Max |
E2 (nmol/L plasma) | 48 b | 0.07 | 0.01 | 0.08 | 0.01 | 0.15 | 32 | 0.37 | 0.07 | 0.22 | 0.09 | 1.67 |
LH (U/L plasma) | 48 c | 3.19 | 0.21 | 3.31 | 0.05 | 7.45 | 32 | 6.98 | 0.63 | 7.01 | 0.14 | 14.96 |
FSH (U/L plasma) | 48 | 2.69 | 0.19 | 2.51 | 0.21 | 5.86 | 32 | 4.48 | 0.39 | 4.59 | 1.14 | 9.57 |
AMH (ng/mL serum) | 54 | 21.9 | 3.78 | 10.86 | 2.45 | 111.32 | 34 | 3.47 | 0.34 | 3.13 | 0.51 | 8.51 |
Inhibin B (pg/mL serum) | 54 | 183.1 | 7.95 | 190.52 | 66.78 | 328.63 | 34 d | 58.28 | 6.87 | 58.86 | 1.46 | 190.43 |
Testosterone (nmol/L plasma) | 48 | 11.37 | 0.91 | 12.20 | 0.27 | 26.93 | ||||||
Free Testosterone (nmol/L plasma) | 48 | 0.22 | 0.02 | 0.23 | 0.00 | 0.58 | ||||||
SHBG (nmol/L plasma) | 48 | 42.80 | 3.04 | 37.60 | 10.90 | 106.50 | ||||||
Albumin (g/L serum) | 54 | 47.49 | 0.28 | 47.50 | 42.70 | 52.20 |
(a) | ||||||||||
Tanner Genital Stage | Testicular Volume | Testosterone | ||||||||
rho | p | rho | p | rho | p | |||||
Tanner Pubic Hair stage | 0.76 | <0.001 | 0.52 | <0.001 | 0.66 | <0.001 | ||||
Tanner Genital Stage | x | x | 0.51 | <0.001 | 0.49 | <0.001 | ||||
Testicular Volume | 0.51 | <0.001 | x | x | 0.42 | 0.004 | ||||
(b) | ||||||||||
Tanner Pubic Hair Stage | Self-Reported Age at Menarche | Self-Reported Age at Onset Breast Growth | Self-Reported Age at Onset of Pubic Hair Growth | Self-Reported Age at Onset Growth Spurt | ||||||
rho | p | rho | p | rho | p | rho | p | rho | P | |
Tanner Breast Stage | 0.46 | 0.003 | −0.25 | 0.154 | −0.19 | 0.241 | −0.10 | 0.537 | −0.21 | 0.232 |
Tanner Pubic hair Stage | x | x | −0.46 | 0.006 | −0.49 | 0.001 | −0.45 | 0.003 | −0.30 | 0.090 |
Free Testosterone | E2 | LH | SHBG | Testicular Volume | Self-Reported Age at Onset Growth Spurt | Tanner Pubic Hair Stage 5 (Compared to 4) | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
beta | p | beta | p | beta | p | beta | p | beta | p | beta | p | beta | p | |
BMI | 0.30 | 0.037 | 0.43 | 0.003 | 0.36 | 0.013 | −0.51 | <0.001 | 0.24 | 0.087 | −0.32 | 0.033 | 0.38 | 0.006 |
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Berghuis, S.A.; Bos, A.F.; Groen, H.; de Jong, W.H.A.; Muller Kobold, A.C.; Wagenmakers-Huizinga, L.; Sauer, P.J.J.; Bocca, G. Prenatal Environmental Exposure to Persistent Organic Pollutants and Reproductive Hormone Profile and Pubertal Development in Dutch Adolescents. Int. J. Environ. Res. Public Health 2022, 19, 9423. https://doi.org/10.3390/ijerph19159423
Berghuis SA, Bos AF, Groen H, de Jong WHA, Muller Kobold AC, Wagenmakers-Huizinga L, Sauer PJJ, Bocca G. Prenatal Environmental Exposure to Persistent Organic Pollutants and Reproductive Hormone Profile and Pubertal Development in Dutch Adolescents. International Journal of Environmental Research and Public Health. 2022; 19(15):9423. https://doi.org/10.3390/ijerph19159423
Chicago/Turabian StyleBerghuis, Sietske A., Arend F. Bos, Henk Groen, Wilhelmina H. A. de Jong, Anneke C. Muller Kobold, Lucie Wagenmakers-Huizinga, Pieter J. J. Sauer, and Gianni Bocca. 2022. "Prenatal Environmental Exposure to Persistent Organic Pollutants and Reproductive Hormone Profile and Pubertal Development in Dutch Adolescents" International Journal of Environmental Research and Public Health 19, no. 15: 9423. https://doi.org/10.3390/ijerph19159423