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. 2002 Aug;110(8):771–776. doi: 10.1289/ehp.02110771

Sexual maturation in relation to polychlorinated aromatic hydrocarbons: Sharpe and Skakkebaek's hypothesis revisited.

Elly Den Hond 1, Harry A Roels 1, Karel Hoppenbrouwers 1, Tim Nawrot 1, Lutgarde Thijs 1, Corinne Vandermeulen 1, Gerhard Winneke 1, Dirk Vanderschueren 1, Jan A Staessen 1
PMCID: PMC1240947  PMID: 12153757

Abstract

Polychlorinated aromatic hydrocarbons (PCAHs) have been described as endocrine disruptors in animals and in accidentally or occupationally exposed humans. In the present study we examined the effect of moderate exposure to PCAHs on sexual maturation. Two hundred adolescents (mean age, 17.4 years) who resided in two polluted suburbs and a rural control area in Flanders (Belgium) participated. We measured the serum concentration of polychlorinated biphenyl (PCB) congeners 138, 153, and 180 and dioxin-like compounds [chemically activated luciferase expression (CALUX) assay] as biomarkers of exposure. School physicians assessed the pubertal development of boys and girls and measured testicular volume. In one suburb near two waste incinerators, compared with the other suburb and the control area, fewer boys (p < 0.001) had reached the adult stages of genital development (62% vs. 92% and 100%, respectively) and pubic hair growth (48% vs. 77% and 100%). Also, in the same suburb, fewer girls (p = 0.04) had reached the adult stage of breast development (67% vs. 90% and 79%). In individual boys, a doubling of the serum concentration of PCB congener 138 increased the odds of not having matured into the adult stage of genital development by 3.5 (p = 0.04); similarly for PCB congener 153 in relation to male pubic hair growth, the odds ratio was 3.5 (p = 0.04). In girls, a doubling of the serum dioxin concentration increased the odds of not having reached the adult stage of breast development by 2.3 (p = 0.02). Left plus right testicular volume was lower in both polluted areas than in the control area (42.4 mL vs. 47.3 mL, p = 0.005) but was not related to the current exposure of the adolescents to PCAHs. Through endocrine disruption, environmental exposure to PCAHs may interfere with sexual maturation and in the long-run adversely affect human reproduction.

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Selected References

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  1. Andersen A. G., Jensen T. K., Carlsen E., Jørgensen N., Andersson A. M., Krarup T., Keiding N., Skakkebaek N. E. High frequency of sub-optimal semen quality in an unselected population of young men. Hum Reprod. 2000 Feb;15(2):366–372. doi: 10.1093/humrep/15.2.366. [DOI] [PubMed] [Google Scholar]
  2. Brouwer A., Ahlborg U. G., Van den Berg M., Birnbaum L. S., Boersma E. R., Bosveld B., Denison M. S., Gray L. E., Hagmar L., Holene E. Functional aspects of developmental toxicity of polyhalogenated aromatic hydrocarbons in experimental animals and human infants. Eur J Pharmacol. 1995 May 26;293(1):1–40. doi: 10.1016/0926-6917(95)90015-2. [DOI] [PubMed] [Google Scholar]
  3. Carlsen E., Giwercman A., Keiding N., Skakkebaek N. E. Evidence for decreasing quality of semen during past 50 years. BMJ. 1992 Sep 12;305(6854):609–613. doi: 10.1136/bmj.305.6854.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dörnberger V., Dörnberger G. Vergleichende Volumetrie des menschlichen Hodens unter besonderer Berücksichtigung der Hodensonographie, Praderorchidometer, Schirrenzirkel und Schublehre. Andrologia. 1987 Sep-Oct;19(5):487–496. [PubMed] [Google Scholar]
  5. Fleming L. E., Bean J. A., Rudolph M., Hamilton K. Cancer incidence in a cohort of licensed pesticide applicators in Florida. J Occup Environ Med. 1999 Apr;41(4):279–288. doi: 10.1097/00043764-199904000-00010. [DOI] [PubMed] [Google Scholar]
  6. Goldman L. R. Chemicals and children's environment: what we don't know about risks. Environ Health Perspect. 1998 Jun;106 (Suppl 3):875–880. doi: 10.1289/ehp.98106875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gray L. E., Jr, Ostby J. S. In utero 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) alters reproductive morphology and function in female rat offspring. Toxicol Appl Pharmacol. 1995 Aug;133(2):285–294. doi: 10.1006/taap.1995.1153. [DOI] [PubMed] [Google Scholar]
  8. Grimvall E., Rylander L., Nilsson-Ehle P., Nilsson U., Strömberg U., Hagmar L., Ostman C. Monitoring of polychlorinated biphenyls in human blood plasma: methodological developments and influence of age, lactation, and fish consumption. Arch Environ Contam Toxicol. 1997 Apr;32(3):329–336. doi: 10.1007/s002449900193. [DOI] [PubMed] [Google Scholar]
  9. Hansen L. G. Stepping backward to improve assessment of PCB congener toxicities. Environ Health Perspect. 1998 Feb;106 (Suppl 1):171–189. doi: 10.1289/ehp.98106s1171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Klein K. O., Baron J., Colli M. J., McDonnell D. P., Cutler G. B., Jr Estrogen levels in childhood determined by an ultrasensitive recombinant cell bioassay. J Clin Invest. 1994 Dec;94(6):2475–2480. doi: 10.1172/JCI117616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Marshall W. A., Tanner J. M. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969 Jun;44(235):291–303. doi: 10.1136/adc.44.235.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Marshall W. A., Tanner J. M. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970 Feb;45(239):13–23. doi: 10.1136/adc.45.239.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mendola P., Buck G. M., Sever L. E., Zielezny M., Vena J. E. Consumption of PCB-contaminated freshwater fish and shortened menstrual cycle length. Am J Epidemiol. 1997 Dec 1;146(11):955–960. doi: 10.1093/oxfordjournals.aje.a009222. [DOI] [PubMed] [Google Scholar]
  14. Mocarelli P., Gerthoux P. M., Ferrari E., Patterson D. G., Jr, Kieszak S. M., Brambilla P., Vincoli N., Signorini S., Tramacere P., Carreri V. Paternal concentrations of dioxin and sex ratio of offspring. Lancet. 2000 May 27;355(9218):1858–1863. doi: 10.1016/S0140-6736(00)02290-X. [DOI] [PubMed] [Google Scholar]
  15. Pauwels A., Cenijn P. H., Schepens P. J., Brouwer A. Comparison of chemical-activated luciferase gene expression bioassay and gas chromatography for PCB determination in human serum and follicular fluid. Environ Health Perspect. 2000 Jun;108(6):553–557. doi: 10.1289/ehp.00108553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Raivio T., Palvimo J. J., Dunkel L., Wickman S., Jänne O. A. Novel assay for determination of androgen bioactivity in human serum. J Clin Endocrinol Metab. 2001 Apr;86(4):1539–1544. doi: 10.1210/jcem.86.4.7329. [DOI] [PubMed] [Google Scholar]
  17. Safe S. H. Endocrine disruptors and human health--is there a problem? An update. Environ Health Perspect. 2000 Jun;108(6):487–493. doi: 10.1289/ehp.00108487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Safe S., Astroff B., Harris M., Zacharewski T., Dickerson R., Romkes M., Biegel L. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) and related compounds as antioestrogens: characterization and mechanism of action. Pharmacol Toxicol. 1991 Dec;69(6):400–409. doi: 10.1111/j.1600-0773.1991.tb01321.x. [DOI] [PubMed] [Google Scholar]
  19. Sager D. B., Girard D. M. Long-term effects on reproductive parameters in female rats after translactational exposure to PCBs. Environ Res. 1994 Jul;66(1):52–76. doi: 10.1006/enrs.1994.1044. [DOI] [PubMed] [Google Scholar]
  20. Sharpe R. M., Skakkebaek N. E. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet. 1993 May 29;341(8857):1392–1395. doi: 10.1016/0140-6736(93)90953-e. [DOI] [PubMed] [Google Scholar]
  21. Svanholm H., Starklint H., Gundersen H. J., Fabricius J., Barlebo H., Olsen S. Reproducibility of histomorphologic diagnoses with special reference to the kappa statistic. APMIS. 1989 Aug;97(8):689–698. doi: 10.1111/j.1699-0463.1989.tb00464.x. [DOI] [PubMed] [Google Scholar]
  22. Swan S. H., Elkin E. P., Fenster L. Have sperm densities declined? A reanalysis of global trend data. Environ Health Perspect. 1997 Nov;105(11):1228–1232. doi: 10.1289/ehp.971051228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Tas S., Lauwerys R., Lison D. Occupational hazards for the male reproductive system. Crit Rev Toxicol. 1996 May;26(3):261–307. doi: 10.3109/10408449609012525. [DOI] [PubMed] [Google Scholar]
  24. Vermeulen A., Verdonck L., Kaufman J. M. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab. 1999 Oct;84(10):3666–3672. doi: 10.1210/jcem.84.10.6079. [DOI] [PubMed] [Google Scholar]
  25. Weidner I. S., Møller H., Jensen T. K., Skakkebaek N. E. Cryptorchidism and hypospadias in sons of gardeners and farmers. Environ Health Perspect. 1998 Dec;106(12):793–796. doi: 10.1289/ehp.98106793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Whorton D., Krauss R. M., Marshall S., Milby T. H. Infertility in male pesticide workers. Lancet. 1977 Dec 17;2(8051):1259–1261. doi: 10.1016/s0140-6736(77)92665-4. [DOI] [PubMed] [Google Scholar]
  27. Wuthe J., Piechotowski I., Papke O., Zier B., Gabrio T., Kramer D., Kouros B., Schwenk M., Pfaff G. First data on background levels of non-ortho and mono-ortho PCBs in blood of residents from southern Germany. Chemosphere. 1996 Feb;32(3):567–574. doi: 10.1016/0045-6535(95)00351-7. [DOI] [PubMed] [Google Scholar]
  28. Yu M. L., Guo Y. L., Hsu C. C., Rogan W. J. Menstruation and reproduction in women with polychlorinated biphenyl (PCB) poisoning: long-term follow-up interviews of the women from the Taiwan Yucheng cohort. Int J Epidemiol. 2000 Aug;29(4):672–677. doi: 10.1093/ije/29.4.672. [DOI] [PubMed] [Google Scholar]

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