Early breast development in girls after prenatal exposure to non-persistent pesticides

International Journal of Andrology

Volumn 35, Issue 3, 2012, Pages 273-282

  Wohlfahrt Veje, C ^a   Andersen, H R ^a   Schmidt, I M ^a   Aksglaede, L ^a   Sorensen K ^a   Juul, A ^a   Jensen, T K ^a,b   Grandjean, P ^b   Skakkebaek N E ^a   Main, K M ^a  

^a Rigshospitalet   (Denmark)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Adrenarche; Early thelarche; Pesticides; Prenatal exposure; Puberty

Indexed keywords

ANDROSTANOLONE; ANDROSTENEDIONE; ESTRADIOL; FOLLITROPIN; INHIBIN A; INHIBIN B; LUTEINIZING HORMONE; MUELLERIAN INHIBITING FACTOR; PESTICIDE; PRASTERONE SULFATE; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE;

ANDROSTENEDIONE BLOOD LEVEL; ARTICLE; BREAST DEVELOPMENT; ESTRADIOL BLOOD LEVEL; FEMALE; FIRST TRIMESTER PREGNANCY; FOLLITROPIN BLOOD LEVEL; HUMAN; LIMIT OF DETECTION; LUTEINIZING HORMONE BLOOD LEVEL; MAJOR CLINICAL STUDY; MATERNAL SMOKING; MENARCHE; MULTIPLE PREGNANCY; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROLACTIN BLOOD LEVEL; PUBERTY; TESTOSTERONE BLOOD LEVEL;

AGRICULTURE; ANDROSTENEDIONE; BREAST; CHILD; FEMALE; HUMANS; INFANT; PESTICIDES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RISK ASSESSMENT;

EID: 84861459259     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2011.01244.x     Document Type: Article

References (39)

1. Aksglaede L, Juul A, Leffers H, Skakkebaek NE & Andersson AM. (2006) The sensitivity of the child to sex steroids: possible impact of exogenous estrogens. Hum Reprod Update 12, 341-349.
2. Aksglaede L, Sorensen K, Petersen JH, Skakkebaek NE & Juul A. (2009) Recent decline in age at breast development: the Copenhagen Puberty Study. Pediatrics 123, 932-939.
3. Andersen CY & Byskov AG. (2006) Estradiol and regulation of anti-Mullerian hormone, inhibin-A, and inhibin-B secretion: analysis of small antral and preovulatory human follicles' fluid. J Clin Endocrinol Metab 91, 4064-4069.
4. Andersen HR, Vinggaard AM, Rasmussen TH, Gjermandsen IM & Bonefeld-Jorgensen EC. (2002) Effects of currently used pesticides in assays for estrogenicity, androgenicity, and aromatase activity in vitro. Toxicol Appl Pharmacol 179, 1-12.
5. Andersen HR, Schmidt IM, Grandjean P, Jensen TK, Budtz-Jorgensen E, Kjaerstad MB, Baelum J, Nielsen JB, Skakkebaek NE & Main KM. (2008) Impaired reproductive development in sons of women occupationally exposed to pesticides during pregnancy. Environ Health Perspect 116, 566-572.
6. Blanck HM, Marcus M, Tolbert PE, Rubin C, Henderson AK, Hertzberg VS, Zhang RH & Cameron L. (2000) Age at menarche and tanner stage in girls exposed in utero and postnatally to polybrominated biphenyl. Epidemiology 11, 641-647.
7. Blystone CR, Furr J, Lambright CS, Howdeshell KL, Ryan BC, Wilson VS, LeBlanc GA & Gray LE Jr. (2007) Prochloraz inhibits testosterone production at dosages below those that affect androgen-dependent organ weights or the onset of puberty in the male Sprague Dawley rat. Toxicol Sci 97, 65-74.
8. Buck Louis GM, Gray LE Jr, Marcus M, Ojeda SR, Pescovitz OH, Witchel SF et al. (2008) Environmental factors and puberty timing: expert panel research needs. Pediatrics 121(Suppl 3), 192-207.
9. Chellakooty M, Schmidt IM, Haavisto AM, Boisen KA, Damgaard IN, Mau C, Petersen JH, Juul A, Skakkebaek NE & Main KM. (2003) Inhibin A, inhibin B, follicle-stimulating hormone, luteinizing hormone, estradiol, and sex hormone-binding globulin levels in 473 healthy infant girls. J Clin Endocrinol Metab 88, 3515-3520.
10. Christiansen S, Scholze M, Dalgaard M, Vinggaard AM, Axelstad M, Kortenkamp A & Hass U. (2009) Synergistic disruption of external male sex organ development by a mixture of four antiandrogens. Environ Health Perspect 117, 1839-1846.
11. Crain DA, Janssen SJ, Edwards TM, Heindel J, Ho SM, Hunt P et al. (2008) Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil Steril 90, 911-940.
12. Davison KK, Susman EJ & Birch LL. (2003) Percent body fat at age 5 predicts earlier pubertal development among girls at age 9. Pediatrics 111, 815-821.
13. De Vries L, Guz-Mark A, Lazar L, Reches A & Phillip M. (2010) Premature thelarche: age at presentation affects clinical course but not clinical characteristics or risk to progress to precocious puberty. J Pediatr 156, 466-471.
14. Den Hond E, Roels HA, Hoppenbrouwers K, Nawrot T, Thijs L, Vandermeulen C, Winneke G, Vanderschueren D & Staessen JA. (2002) Sexual maturation in relation to polychlorinated aromatic hydrocarbons: Sharpe and Skakkebaek's hypothesis revisited. Environ Health Perspect 110, 771-776.
15. Dennedy MC, Smith D, O'Shea D & McKenna TJ. (2010) Investigation of patients with atypical or severe hyperandrogenaemia including androgen-secreting ovarian teratoma. Eur J Endocrinol 162, 213-220.
16. Dumesic DA, Patankar MS, Barnett DK, Lesnick TG, Hutcherson BA & Abbott DH. (2009) Early prenatal androgenization results in diminished ovarian reserve in adult female rhesus monkeys. Hum Reprod 24, 3188-3195.
17. Euling SY, Herman-Giddens ME, Lee PA, Selevan SG, Juul A, Sorensen TI, Dunkel L, Himes JH, Teilmann G & Swan SH. (2008a) Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics 121(Suppl 3), 172-191.
18. Euling SY, Selevan SG, Pescovitz OH & Skakkebaek NE. (2008b) Role of environmental factors in the timing of puberty. Pediatrics 121(Suppl 3), 167-171.
19. Goetz AK, Ren H, Schmid JE, Blystone CR, Thillainadarajah I, Best DS et al. (2007) Disruption of testosterone homeostasis as a mode of action for the reproductive toxicity of triazole fungicides in the male rat. Toxicol Sci 95, 227-239.
20. Hagen CP, Aksglaede L, Sorensen K, Main KM, Boas M, Cleemann L et al. (2010) Serum levels of anti-Mullerian hormone as a marker of ovarian function in 926 healthy females from birth to adulthood and in 172 Turner syndrome patients. J Clin Endocrinol Metab 95, 5003-5010.
21. Hansen E. (1982) The distribution of living conditions in Denmark. The Danish National Institue of Social research
22. van Houten EL, Themmen AP & Visser JA. (2010) Anti-Mullerian hormone (AMH): regulator and marker of ovarian function. Ann Endocrinol (Paris) 71, 191-197.
23. Kaplowitz P. (2004) Clinical characteristics of 104 children referred for evaluation of precocious puberty. J Clin Endocrinol Metab 89, 3644-3650.
24. Larsen T. (2001) Intrauterine growth restriction Identification, correlation and causation evaluated by use of ultrasound. Dan Med Bull 48, 256-274.
25. Marsal K, Persson PH, Larsen T, Lilja H, Selbing A & Sultan B. (1996) Intrauterine growth curves based on ultrasonically estimated foetal weights. Acta Paediatr 85, 843-848.
26. Marshall WA & Tanner JM. (1969) Variations in pattern of pubertal changes in girls. Arch Dis Child 44, 291-303.
27. Meinhardt U & Mullis PE. (2002) The aromatase cytochrome P-450 and its clinical impact. Horm Res 57, 145-152.
28. Mitamura R, Yano K, Suzuki N, Ito Y, Makita Y & Okuno A. (2000) Diurnal rhythms of luteinizing hormone, follicle-stimulating hormone, testosterone, and estradiol secretion before the onset of female puberty in short children. J Clin Endocrinol Metab 85, 1074-1080.
29. Mouritsen A, Aksglaede L, Sørensen K, Sloth MogensenS, Leffers H, Main K, Frederiksen H, Andersson A, Skakkebaek N & Juul A. (2010) Hypothesis: exposure to endocrine-disruting chemicals may interfere with timing of puberty. Int J Androl 33, 346-359.
30. Norjavaara E, Ankarberg C & Albertsson-Wikland K. (1996) Diurnal rhythm of 17 beta-estradiol secretion throughout pubertal development in healthy girls: evaluation by a sensitive radioimmunoassay. J Clin Endocrinol Metab 81, 4095-4102.
31. Ouyang F, Perry MJ, Venners SA, Chen C, Wang B, Yang F et al. (2005) Serum DDT, age at menarche, and abnormal menstrual cycle length. Occup Environ Med 62, 878-884.
32. Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J & Bourguignon JP. (2003) The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 24, 668-693.
33. Rockett JC, Narotsky MG, Thompson KE, Thillainadarajah I, Blystone CR, Goetz AK et al. (2006) Effect of conazole fungicides on reproductive development in the female rat. Reprod Toxicol 22, 647-658.
34. Roy JR, Chakraborty S & Chakraborty TR. (2009) Estrogen-like endocrine disrupting chemicals affecting puberty in humans - a review. Med Sci Monit 15, 137-145.
35. Schmidt IM, Chellakooty M, Haavisto AM, Boisen KA, Damgaard IN, Steendahl U, Toppari J, Skakkebaek NE & Main KM. (2002) Gender difference in breast tissue size in infancy: correlation with serum estradiol. Pediatr Res 52, 682-686.
36. Taxvig C, Hass U, Axelstad M, Dalgaard M, Boberg J, Andeasen HR & Vinggaard AM. (2007) Endocrine-disrupting activities in vivo of the fungicides tebuconazole and epoxiconazole. Toxicol Sci 100, 464-473.
37. Vasiliu O, Muttineni J & Karmaus W. (2004) In utero exposure to organochlorines and age at menarche. Hum Reprod 19, 1506-1512.
38. Wohlfahrt-Veje C, Main KM, Schmidt IM, Boas M, Jensen TK, Grandjean P, Skakkebaek NE & Andersen HR. (2011) Lower birth weight and increased body fat at school age in children prenatally exposed to modern pesticides: a prospective study. Environ Health 10, 79.
39. Wu XY, Li ZL, Wu CY, Liu YM, Lin H, Wang SH & Xiao WF. (2010) Endocrine traits of polycystic ovary syndrome in prenatally androgenized female Sprague-Dawley rats. Endocr J 57, 201-209.