Prenatal and peripubertal phthalates and bisphenol A in relation to sex hormones and puberty in boys

Reproductive Toxicology

Volumn 47, Issue , 2014, Pages 70-76

  Ferguson, Kelly K ^a   Peterson, Karen E ^a,b   Lee, Joyce M ^a   Mercado García, Adriana ^c   Blank Goldenberg, Clara ^d   Téllez Rojo, Martha M ^c   Meeker, John D ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^d AMERICAN BRITISH COWDRAY MEDICAL CENTER   (Mexico)

Author keywords

Bisphenol A; Environment; Exposure; Puberty; Tanner stage; Testosterone

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTRADIOL; INHIBIN B; PHTHALIC ACID DERIVATIVE; PRASTERONE SULFATE; SEX HORMONE; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE; BENZHYDRYL DERIVATIVE; INHIBIN; PHENOL DERIVATIVE; PHTHALIC ACID; POLLUTANT; MONO CARBOXYPROPYL PHTHALATE; MONO ETHYL PHTHALATE; MONO ISOBUTYL PHTHALATE; MONO N BUTYL PHTHALATE; MONO(2 ETHYL 5 HYDROXYHEXYL)PHTHALATE; MONO(2 ETHYL 5 OXOHEXYL)PHTHALATE; MONOBENZYL PHTHALATE; PHTHALIC ACID 2 ETHYLHEXYL MONOESTER; UNCLASSIFIED DRUG;

ADRENARCHE; ADULT; ARTICLE; BLOOD ANALYSIS; CHILD; CHILD DEVELOPMENT; CHILD HEALTH; CONTROLLED STUDY; CORRELATIONAL STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; ENVIRONMENTAL EXPOSURE; FEMALE; GESTATIONAL AGE; HORMONE BLOOD LEVEL; HUMAN; LIMIT OF DETECTION; MALE; METABOLITE; PRENATAL EXPOSURE; PRENATAL PERIOD; PUBERTY; SEX DIFFERENCE; THIRD TRIMESTER PREGNANCY; UPREGULATION; URINALYSIS; ADOLESCENT; ANATOMY AND HISTOLOGY; BLOOD; ENVIRONMENTAL MONITORING; MALE GENITAL SYSTEM; POLLUTANT; PREGNANCY; URINE; CROSS-SECTIONAL STUDY; LONGITUDINAL STUDY; REPRODUCTIVE TOXICITY; SCHOOL CHILD; SEXUAL DEVELOPMENT; TESTIS SIZE;

ADOLESCENT; BENZHYDRYL COMPOUNDS; CHILD; DEHYDROEPIANDROSTERONE SULFATE; ENVIRONMENTAL MONITORING; ENVIRONMENTAL POLLUTANTS; ESTRADIOL; FEMALE; GENITALIA, MALE; HUMANS; INHIBINS; MALE; PHENOLS; PHTHALIC ACIDS; PREGNANCY; PREGNANCY TRIMESTER, THIRD; PRENATAL EXPOSURE DELAYED EFFECTS; PUBERTY; SEX HORMONE-BINDING GLOBULIN; TESTOSTERONE;

EID: 84903724883     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2014.06.002     Document Type: Article

References (58)

1. Meeker J.D., Sathyanarayana S., Swan S.H. Phthalates and other additives in plastics: human exposure and associated health outcomes. Philos Trans R Soc Lond B Biol Sci 2009, 364(1526):2097-2113.
2. Rochester J.R. Bisphenol A and human health: a review of the literature. Reprod Toxicol 2013, 42C:132-155.
3. Wittassek M., Koch H.M., Angerer J., Bruning T. Assessing exposure to phthalates - the human biomonitoring approach. Mol Nutr Food Res 2011, 55(1):7-31.
4. Geens T., Aerts D., Berthot C., Bourguignon J.P., Goeyens L., Lecomte P., et al. A review of dietary and non-dietary exposure to bisphenol-A. Food Chem Toxicol. 2012, 50(10):3725-3740.
5. Zoeller R.T., Brown T.R., Doan L.L., Gore A.C., Skakkebaek N.E., Soto A.M., et al. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology 2012, 153(9):4097-4110.
6. Meeker J.D. Exposure to environmental endocrine disrupting compounds and men's health. Maturitas 2010, 66(3):236-241.
7. Sathyanarayana S., Barrett E., Butts S., Wang C.W., Swan S. Phthalate exposure and reproductive hormone concentrations in pregnancy. Reproduction 2014, 147(4):401-409.
8. Gonzalez-Cossio T., Peterson K.E., Sanin L.H., Fishbein E., Palazuelos E., Aro A., et al. Decrease in birth weight in relation to maternal bone-lead burden. Pediatrics 1997, 100(5):856-862.
9. Hu H., Tellez-Rojo M.M., Bellinger D., Smith D., Ettinger A.S., Lamadrid-Figueroa H., et al. Fetal lead exposure at each stage of pregnancy as a predictor of infant mental development. Environ Health Perspect 2006, 114(11):1730-1735.
10. Lewis R.C., Meeker J.D., Peterson K.E., Lee J.M., Pace G.G., Cantoral A., et al. Predictors of urinary bisphenol A and phthalate metabolite concentrations in Mexican children. Chemosphere 2013, 93(10):2390-2398.
11. Braun J.M., Sathyanarayana S., Hauser R. Phthalate exposure and children's health. Curr Opin Pediatr 2013, 25(2):247-254.
12. Rochester J.R. Bisphenol A and human health: a review of the literature. Reprod Toxicol 2013, 42:132-155.
13. Silva M.J., Samandar E., Preau J.L., Reidy J.A., Needham L.L., Calafat A.M. Quantification of 22 phthalate metabolites in human urine. J Chromatogr B Analyt Technol Biomed Life Sci 2007, 860(1):106-112.
14. Hornung R.W., Reed L. Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg 1990, 5:46-51.
15. 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, 84(10):3666-3672.
16. Marshall W.A., Tanner J.M. Variations in the pattern of pubertal changes in boys. Arch Dis Child 1970, 45(239):13-23.
17. Herman-Giddens M.E., Wang L., Koch G. Secondary sexual characteristics in boys: estimates from the national health and nutrition examination survey III, 1988-1994. Arch Pediatr Adolesc Med 2001, 155(9):1022-1028.
18. Mouritsen A., Aksglaede L., Soerensen K., Hagen C.P., Petersen J.H., Main K.M., et al. The pubertal transition in 179 healthy Danish children: associations between pubarche, adrenarche, gonadarche, and body composition. Eur J Endocrinol 2013, 168(2):129-136.
19. WHO Reference 2007: Growth reference data for 5-19 years 2007, http://www.who.int/growthref/en/.
20. Hauser R., Sergeyev O., Korrick S., Lee M.M., Revich B., Gitin E., et al. Association of blood lead levels with onset of puberty in Russian boys. Environ Health Perspect 2008, 116(7):976-980.
21. Fisher J.S., Macpherson S., Marchetti N., Sharpe R.M. Human 'testicular dysgenesis syndrome': a possible model using in-utero exposure of the rat to dibutyl phthalate. Hum Reprod 2003, 18(7):1383-1394.
22. Shultz V.D., Phillips S., Sar M., Foster P.M., Gaido K.W. Altered gene profiles in fetal rat testes after in utero exposure to di(n-butyl) phthalate. Toxicol Sci 2001, 64(2):233-242.
23. Foster P.M. Disruption of reproductive development in male rat offspring following in utero exposure to phthalate esters. Int J Androl 2006, 29(1):140-147. discussion 181-145.
24. Swan S.H. Environmental phthalate exposure in relation to reproductive outcomes and other health endpoints in humans. Environ Res 2008, 108(2):177-184.
25. Swan S.H., Main K.M., Liu F., Stewart S.L., Kruse R.L., Calafat A.M., et al. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect 2005, 113(8):1056-1061-
26. Ormond G., Neiuwenhuijsen M.J., Nelson P., Toledano M.B., Iszatt N., Geneletti S., et al. Endocrine disruptors in the workplace, hair spray, folate supplementation, and risk of hypospadias: case-control study. Environ Health Perspect 2009, 117(2):303-307.
27. Suzuki Y., Yoshinaga J., Mizumoto Y., Serizawa S., Shiraishi H. Foetal exposure to phthalate esters and anogenital distance in male newborns. Int J Androl 2012, 35(3):236-244.
28. Main K.M., Mortensen G.K., Kaleva M.M., Boisen K.A., Damgaard I.N., Chellakooty M., et al. Human breast milk contamination with phthalates and alterations of endogenous reproductive hormones in infants three months of age. Environ Health Perspect 2006, 114(2):270-276.
29. Associations between maternal phthalate exposure and cord sex hormones in human infants. Chemosphere 2011, 83(8):1192-1199.
30. Biro F.M., Lucky A.W., Huster G.A., Morrison J.A. Pubertal staging in boys. J Pediatr 1995, 127(1):100-102.
31. In utero exposure to di-(2-ethylhexyl) phthalate exerts both short-term and long-lasting suppressive effects on testosterone production in the rat. Biol Reprod 2008, 78(6):1018-1028.
32. Martinez-Arguelles D.B., Guichard T., Culty M., Zirkin B.R., Papadopoulos V. In utero exposure to the antiandrogen di-(2-ethylhexyl) phthalate decreases adrenal aldosterone production in the adult rat. Biol Reprod 2011, 85(1):51-61.
33. Martinez-Arguelles D.B., Campioli E., Culty M., Zirkin B.R., Papadopoulos V. Fetal origin of endocrine dysfunction in the adult: the phthalate model. J Steroid Biochem Mol Biol 2013.
34. Buck Louis G.M., Gray L.E., Marcus M., Ojeda S.R., Pescovitz O.H., Witchel S.F., et al. Environmental factors and puberty timing: expert panel research needs. Pediatrics 2008, 121(Suppl. 3):S192-S207.
35. Alonso-Magdalena P., Ropero A.B., Soriano S., Garcia-Arevalo M., Ripoll C., Fuentes E., et al. isphenol-A acts as a potent estrogen via non-classical estrogen triggered pathways. Mol Cell Endocrinol 2012, 355(2):201-207.
36. Lee H.J., Chattopadhyay S., Gong E.Y., Ahn R.S., Lee K. Antiandrogenic effects of bisphenol A and nonylphenol on the function of androgen receptor. Toxicol Sci 2003, 75(1):40-46.
37. Comparative study of the endocrine-disrupting activity of bisphenol A and 19 related compounds. Toxicol Sci 2005, 84(2):249-259.
38. Sohoni P., Sumpter J.P. Several environmental oestrogens are also anti-androgens. J Endocrinol 1998, 158(3):327-339.
39. In utero exposure to bisphenol-A and anogenital distance of male offspring. Birth Defects Res A Clin Mol Teratol 2011, 91(10):867-872.
40. Christiansen S., Axelstad M., Boberg J., Vinggaard A.M., Pedersen G.A., Hass U. Low-dose effects of bisphenol A on early sexual development in male and female rats. Reproduction 2014, 147(4):477-487.
41. Kobayashi K., Miyagawa M., Wang R.S., Sekiguchi S., Suda M., Honma T. Effects of in utero and lactational exposure to bisphenol A on somatic growth and anogenital distance in F1 rat offspring. Ind Health 2002, 40(4):375-381.
42. Unconjugated bisphenol A cord blood levels in boys with descended or undescended testes. Hum Reprod 2012, 27(4):983-990.
43. Effect of prenatal exposure to bisphenol A on the serum testosterone concentration of rats at birth. Hum Exp Toxicol 2006, 25(7):369-373.
44. Imbalance of testosterone level in male offspring of rats perinatally exposed to bisphenol A. Ind Health 2003, 41(4):338-341.
45. Temporal variability in urinary excretion of bisphenol A and seven other phenols in spot, morning, and 24-h urine samples. Environ Res 2013.
46. A mixture of five phthalate esters inhibits fetal testicular testosterone production in the Sprague-Dawley rat in a cumulative, dose-additive manner. Toxicol Sci 2008, 105(1):153-165.
47. Lehmann K.P., Phillips S., Sar M., Foster P.M., Gaido K.W. Dose-dependent alterations in gene expression and testosterone synthesis in the fetal testes of male rats exposed to di (n-butyl) phthalate. Toxicol Sci 2004, 81(1):60-68.
48. Mylchreest E., Sar M., Wallace D.G., Foster P.M. Fetal testosterone insufficiency and abnormal proliferation of Leydig cells and gonocytes in rats exposed to di(n-butyl) phthalate. Reprod Toxicol 2002, 16(1):19-28.
49. Plasma phthalate levels in pubertal gynecomastia. Pediatrics 2010, 125(1):e122-e129.
50. Misuse of blood serum to assess exposure to bisphenol A and phthalates. Breast Cancer Res 2013, 15(5):403.
51. Urinary phthalate excretion in 555 healthy Danish boys with and without pubertal gynaecomastia. Int J Androl 2012, 35(3):227-235.
52. Mouritsen A., Frederiksen H., Sorensen K., Aksglaede L., Hagen C., Skakkebaek N.E., et al. Urinary phthalates from 168 girls and boys measured twice a year during a 5 year period: associations with adrenal androgen levels and puberty. J Clin Endocrinol Metab 2013.
53. Phthalate excretion pattern and testicular function: a study of 881 healthy Danish men. Environ Health Perspect 2012, 120(10):1397-1403.
54. Meeker J.D., Calafat A.M., Hauser R. Urinary metabolites of di(2-ethylhexyl) phthalate are associated with decreased steroid hormone levels in adult men. J Androl 2009, 30(3):287-297.
55. Meeker J.D., Calafat A.M., Hauser R. Urinary bisphenol A concentrations in relation to serum thyroid and reproductive hormone levels in men from an infertility clinic. Environ Sci Technol 2010, 44(4):1458-1463.
56. Are environmental levels of bisphenol a associated with reproductive function in fertile men?. Environ Health Perspect 2010, 118(9):1286-1291.
57. Serum bisphenol-A concentration and sex hormone levels in men. Fertil Steril 2013, 100(2):478-482.
58. Daily bisphenol A excretion and associations with sex hormone concentrations: results from the InCHIANTI adult population study. Environ Health Perspect 2010, 118(11):1603-1608.