Exposure to endocrine disrupting chemicals and male reproductive health

Frontiers in Public Health

Volumn 2, Issue JUN, 2014, Pages

  Jeng, Hueiwang Anna ^a  

^a OLD DOMINION UNIVERSITY   (United States)

Author keywords

Bisphenol A; Dichlorodiphenyldichloroethylene; Endocrine disruptors; Trichloroethane

Indexed keywords

EID: 84915762142     PISSN: None     EISSN: 22962565     Source Type: Journal    
DOI: 10.3389/fpubh.2014.00055     Document Type: Review

References (111)

1. Kavlock RJ, Daston GP, DeRosa C, Fenner-Crisp P, Gray LE, Kaattari S, et al. Research needs for the risk assessment of health and environmental effects of endocrine disruptors: a report of the U.S. EPA-sponsored workshop. Environ Health Perspect (1996) 104:715-40. doi:10.1289/ehp.96104s4715
2. Nash JP, Kime DE, Van der Ven LTM, Wester PW, Brion F, Maack G, et al. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ Health Perspect (2004) 112:1725-33. doi:10.1289/ehp.7209
3. Swan SH, Elkin EP, Fenster L. The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ Health Perspect (2000) 108:961-6. doi:10.1289/ehp.00108961
4. Travison TG, Araujo AB, O'Donnell AB, Kupelian V, McKinlay JB. A population-level decline in serum testosterone levels in American men. J Clin Endocrinol Metab (2007) 92:196-202. doi:10.1210/jc.2006-1375
5. Kania-Korwel I, El-Komy MH, Veng-Pedersen P, Lehmler HJ. Clearance of polychlorinated biphenyl atropisomers is enantioselective in female C57Bl/6 mice. Environ Sci Technol (2010) 44:2828-35. doi:10.1021/es901781p
6. NorstromK,CzubG,McLachlan MS,Hu D,ThornePS, Hornbuckle KC. External exposure and bioaccumulationof PCBsinhumans livinginacontaminated urban environment. Environ Int (2010) 36:855-61. doi:10.1016/j.envint.2009. 03.005
7. Turusov V, Rakitsky V, Tomatis L. Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence and risks. Res Rev (2002) 110(2):125-8.
8. Bhatia R, Shiau R, Petreas M, Weintraub JM, Farhang L, Eskenazi B. Organochlorine pesticides and male genital anomalies in the child health and development studies. Environ Health Perspect (2005) 113(2):220-4. doi:10. 1289/ehp.7382
9. Edwards TM, Moore BC, Guillette LJ Jr. Reproductive dysgenesis in wildlife: a comparative view. Int J Androl (2006) 29:109-21. doi:10.1111/j.1365-2605. 2005.00631.x
10. Guillette LJ Jr, Moore BC. Environmental contaminants, fertility, and multioocytic follicles: a lesson from wildlife? Semin Reprod Med (2006) 24:134-41. doi:10.1055/s-2006-944419
11. Kilian E, Delport R, Bornman MS, de Jager C. Simultaneous exposure to low concentrations of DDT, deltamethrin, phytoestrogens and nonylphenol harms reproductive parameters in male rats. Andrologia (2007) 39:128-35. doi:10.1111/j.1439-0272.2007.00777.x
12. Rignell-Hydbom A, Rylander L, Giwercman A, Jönsson BAG, Nilsson-Ehle P, HagmarL.ExposuretoCB-153and p,p0-DDE and malereproductivefunction. Hum Reprod (2004) 19:2066-75. doi:10.1093/humrep/deh362
13. de Jager C, Farias P, Barraza-Villarreal A, Avila MH, Ayotte P, Dewailly E, et al. Reduced seminal parameters associated with environmental DDT exposure and p,p0-DDE concentrations in men in Chiapas, Mexico: a cross-sectional study. J Androl (2006) 27:16-27. doi:10.2164/jandrol.05121
14. Toft G,Rignell-Hydbom A,Tyrkiel E,Shvets M,Giwercman A,Lindh CH,et al. Semen quality and exposure to persistent organochlorine pollutants. Epidemiology (2006) 17:450-8. doi:10.1097/01.ede.0000221769.41028.d2
15. Hauser R, Chen Z, Pothier L, Ryan L, Altshul L. The relationship between human semen parameters and environmental exposure to polychlorinated biphenyls and p,p'-DDE. Environ Health Perspect (2003) 111(12):1505-11. doi:10.1289/ehp.6175
16. Biles JE, McNeal TP, Begley TH, Hollifield HC. Determination of bisphenol-A in reusable polycarbonate food-contact plastics and migration to food simulating liquids. J Agric Food Chem (1997) 45:3541-4. doi:10.1021/jf970072i
17. Agency for Toxic Substances & Disease Registry (ATSDR). Toxicological Profile for Di(2-Ethylnexyl) Phthalate (DEHP). Washington, DC: U.S. Department of Health and Human Services (2002).
18. Aly HA, Domenech O,Abdel-Naim AB. Aroclor 1254 impairs spermatogenesis and induces oxidative stress in rat testicular mitochondria. Food Chem Toxicol (2009) 47:1733-8. doi:10.1016/j.fct.2009.03.019
19. Hauser R,Altshul L, Chen Z, Ryan L, Overstreet J, Schiff I, et al. Environmental organochlorines and semen quality: results of a pilot study. Environ Health Perspect (2002) 110:229-33. doi:10.1289/ehp.02110229
20. Bonde JP,ToftG,RylanderL,Rignell-HydbomA,GiwercmanA,Spano M,et al. Fertility andmarkersof male reproductive functioninInuit and European pop-ulations spanning large contrasts in blood levels of persistent organochlorines. Environ Health Perspect (2008) 116:269-77. doi:10.1289/ehp.10700
21. Pant N, Manju S, Kumar Patel D, Shukla Y, Mathur N, Kumar Gupta Y, et al. Correlation of phthalate exposures with semen quality. Toxicol Appl Pharmacol (2008) 231(1):112-6. doi:10.1016/j.taap.2008.04.001
22. Pant N, Pant AB, Shukla M, Mathur N, Gupta YK, Saxena DK. Envi-ronmental and experimental exposure of phthalate esters: the toxicologi-cal consequence on human sperm. Hum Exp Toxicol (2011) 30(6):507-14. doi:10.1177/0960327110374205
23. Duty SM, Silva MJ, Barr DB, Brock JW, Ryan L, Chen Z, et al. Phthalate exposure and human semen parameters. Epidemiology (2003) 14:269-77. doi:10.1097/01.EDE.0000059950.11836.16
24. Hauser R, Meeker JD, Duty S, Silva MJ, Calafat AM. Altered semen quality in relation to urinary concentrations of phthalate monoester and oxidative metabolites. Epidemiology (2006) 17:682-91. doi:10.1097/01.ede.0000235996. 89953.d7
25. Wirth JJ, Rossano MG, Potter R, Puscheck E, Daly DC, Paneth N, et al. A pilot study associating urinary concentrations of phthalate metabolites and semen quality. Syst Biol Reprod Med (2008) 54(3):143-54. doi:10.1080/ 19396360802055921
26. Jurewicz J, Radwan M, Sobala W, Ligocka D, Radwan P, Bochenek M, et al. Human urinaryphthalate metabolites level and main semen parameters,sperm chromatin structure, sperm aneuploidy and reproductive hormones. Reprod Toxicol (2013) 42:232-41. doi:10.1016/j.reprotox.2013.10.001
27. Meeker JD, Ehrlich S, Toth TL, Wright DL, Calafat AM, Trisini AT, et al. Semen quality and sperm DNA damage in relation to urinary bisphenol A among men from an infertility clinic. Reprod Toxicol (2010) 30:532-9. doi:10.1016/j.reprotox.2010.07.005
28. Mendiola J, Jørgensen N, Andersson AM, Calafat AM, Ye X, Redmon JB, et al. Are environmental levels of bisphenol A associated with reproductive function in fertile men? Environ Health Perspect (2010) 118:1286-91. doi:10.1289/ehp.1002037
29. Mendiola J, Jørgensen N, Andersson A, Calafat A, Silva M, Redmon J, et al. Associations between urinary metabolites of di(2-ethylhexyl)phthalate and reproductive hormones in fertile men. Int J Androl (2010) 14:1-10. doi:10.1111/j.1365-2605.2010.01095.x
30. Li DK, Zhou Z, Miao M, He Y, Wang J, Ferber J, et al. Urine bisphenol-A (BPA) level in relation to semen quality. Fertil Steril (2011) 95(2):625-30. doi:10.1016/j.fertnstert.2010.09.026
31. Knez J, Kranvogl R, Breznik BP, Voncina E, Vlaisavljevic V. Are urinary bisphenol A levels in men related to semen quality and embryo development after medically assisted reproduction? Fertil Steril (2013) 101(1):215.e-21.e. doi:10.1016/j.fertnstert.2013.09.030
32. Hauser R, Williams P, Altshul L, Calafat AM. Evidence of interaction between polychlorinated biphenyls and phthalates in relation to human sperm motility. Environ Health Perspect (2005) 113(4):425. doi:10.1289/ehp.7305
33. Aneck-Hahn NH, Schulenburg GW, Bornman MS, Farias P, de Jager C. Impairedsemenqualityassociatedwith environmentalDDT exposureinyoung men living in a malaria area in the Limpopo Province, South Africa. J Androl (2007) 28:423-34. doi:10.2164/jandrol.106.001701
34. Ayotte P, Giroux S, Dewailly E, Hernández Avila M, Farias P, Danis R, et al. DDT spraying for malaria control and reproductive function in Mexican men. Epi (2001) 12(3):366-7.
35. Charlier CJ, Foidart JM. Comparative study of dichlorodiphenyldichloroethyl-ene in blood and semen of two young male populations: lack of relationship to infertility, but evidence of high exposure of the mothers. Reprod Toxicol (2005) 20(2):215-20.
36. Duty SM, Singh NP, Silva MJ, Barr DB, Brock JW, Ryan L, et al. The relationship between environmental exposures to phthalates and DNA damage in human sperm using the neutral comet assay. Environ Health Perspect (2003) 111:1164-9. doi:10.1289/ehp.5756
37. Hauser R, Meeker JD, Singh NP, Silva MJ, Ryan L, Duty S, et al. DNA damage in human sperm is related to urinary levels of phthalate monoester and oxidativemetabolites.Hum Repro d (2007) 22(3):688-95. doi:10.1093/humrep/ del428
38. Meeker JD, Yang T, Ye X, Calafat AM, Hauser R. Urinary concentrations of parabens and serum hormone levels, semen quality parameters, and sperm DNA damage. Environ Health Perspect (2011) 119(2):252-7. doi:10.1289/ehp. 1002238
39. Hauser R, Singh NP, Chen Z, Pothier L, Altshul L. Lack of an association between environmental exposure to polychlorinated biphenyls and p,p'-DDE and DNA damage in human sperm measured using the neutral comet assay. Hum Reprod (2003) 18(12):2525-33. doi:10.1093/humrep/deg508
40. Spanò M,Seli E,Bizzaro D,Manicardi GC, Sakkas D. The significance of sperm nuclear DNAstrandbreaksonreproductiveoutcome.Curr OpinObstetGynecol (2005) 17:255-60. doi:10.1097/01.gco.0000169102.77504.66
41. Spanò M, Toft G, Hagmar L, Eleuteri P, Rescia M, Rignell-Hydbom A, et al. Exposure to PCB and p, p'-DDE in European and Inuit populations: impact on human sperm chromatin integrity. Hum Reprod (2005) 20(12):3488-99. doi:10.1093/humrep/dei297
42. Giwercman YL, Kleist KE, Giwercman A,Giwercman C,Toft G,Bonde JP, et al. Remarkably low incidence of hypospadias in Greenland despite high exposure to endocrine disrupters: possible protective effect of androgen receptor genotype. Pharmacogenet Genomics (2006) 16(5):375-7. doi:10.1097/01.fpc. 0000199497.01101.93
43. Al-Hiyasat AS, Darmani H. In vivo effects of BISGMA-a component of dental composite-on male mouse reproduction and fertility. J Biomed Mater Res A (2006)78:66-72. doi:10.1002/jbm.a.30667
44. Furuya M, Adachi K, Kuwahara S, Ogawa K, Tsukamoto Y. Inhibition of male chick phenotypes and spermatogenesis by bisphenol-A. Life Sci (2006) 78:1767-76.
45. Xiao GB, Wang RY, Cai YZ, He GH, Zhou ZJ. Effect of bisphenol A on semen quality of exposed workers: a pilot study. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi (2009) 27(12):741-3.
46. Srivastava S, Singh GB, Srivastava SP, Seth PK. Testicular toxicity of di-n-butyl phthalate in adult rats: effect on marker enzymes of spermatogenesis. Indian J Exp Biol (1990) 28:67-70.
47. Park JD, Sultan SMH, Klaassen CD. Testicular toxicity of di-(2 ethylhexyl) phthalate in young Sprague-Dawley rats. Toxicology (2002) 171:105-15. doi: 10.1016/S0300-483X(01)00567-4
48. Duty S, Calafat AM, Silva MJ, Brock JW, Ryan L, Chen Z, et al. The relationship betweenenvironmental exposuretophthalates andcomputer-aidedsperm analysis motion parameters. J Androl (2004) 25(2):293-302.
49. Hauser R, Sergeyev O, Korrick S, Lee MM, Revich B, Gitin E, et al. Association of blood lead levels with onset of puberty in Russian boys. Environ Health Perspect (2008) 116:976-80. doi:10.1289/ehp.10516
50. Jönsson AG, Richthoff J, Rylande L, Giwercman A, Lars H. Urinary phthalate metabolites and biomarkers of reproductive function in young men. Epidemiology (2005) 16(4):487-93. doi:10.1097/01.ede.0000164555.19041.01
51. Aitken RJ, De Iuliis GN. On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod (2010) 16:3-13. doi:10.1093/molehr/gap059
52. Rignell-HydbomA,Rylander L,GiwercmanA,Jönsson BA, LindhC,EleuteriP, et al. Exposure to PCBs and p,p'-DDE and human sperm chromatin integrity. Environ Health Perspect (2005) 113:175-9. doi:10.1289/ehp.7252
53. Stronati A, Manicardi GC, Cecati M,Bordicchia M, Ferrante L, Spanò M, et al. Relationships between sperm DNA fragmentation, sperm apoptotic markers and serum levels of CB-153 and p,p'-DDE in European and Inuit populations. Reproduction (2006) 132(6):949-58. doi:10.1530/rep.1.01034
54. Bungum M, Humaidan P, Axmon A, Spanó M, Bungum L, Erenpreiss J, et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod (2007) 22:174-9. doi:10.1093/humrep/ del326
55. Rozati R, Reddy PP, Reddanna P, Mujtaba R. Role of environmental estrogens in the deterioration of male factor fertility. Fertil Steril (2002) 78:1187-94. doi:10.1016/S0015-0282(02)04389-3
56. de Jager C, Aneck-Hahn NH, Bornman MS, Farias P, Leter G, Eleuteri P, et al. Sperm chromatin integrityinDDT-exposed young men livingin a malaria area in the Limpopo Province, South Africa. Hum Reprod (2009) 24(10):2429-38. doi:10.1093/humrep/dep249
57. Takahashi S, Chi XJ, Yamaguchi Y, Suzuki H, Sugaya S, Kita K. Mutagenicity of bisphenol l A and its suppression by interferon-alpha in human RSa cells. Mutat Res (2001) 490:199-207. doi:10.1016/S1383-5718(00)00161-3
58. Iso T,Watanabe T,Iwamoto T, Shimamoto A, FuruichiY. DNA damage caused by bisphenol A and estradiol through estrogenic activity. Biol Pharm Bull (2006) 29:206-10.
59. Meeker JD, Calafat AM, 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) 44:1458-63. doi:10.1021/es9028292
60. Han X, Cui Z, Zhou N, Ma M, Li L, Li Y, et al. Urinary phthalate metabolites and male reproductive function parameters in Chongqing general population, China. Int J Hyg Environ Health (2014) 217(2-3):271-8. doi:10.1016/j.ijheh. 2013.06.006
61. Hutson JM,BalicA,NationT,SouthwellB.Cryptorchidism. Semin Pediatr Surg (2010) 19(3):215-24. doi:10.1053/j.sempedsurg.2010.04.001
62. Hosie S, Loff S, Witt K, Niessen K, Waag KL. Is there a correlation between organochlorine compounds and undescended testes? Eur J Pediatr Surg (2000) 10(5):304-9. doi:10.1055/s-2008-1072381
63. Mol NM, Sorensen N, Weihe P, Andersson AM, Jorgensen N, Skakkebaek NE, et al. Spermaturia and serum hormone concentrations at the age of puberty in boys prenatally exposed to polychlorinated biphenyls. Eur J Endocrinol (2002) 146:357-63. doi:10.1530/eje.0.1460357
64. Brucker-Davis F, Wagner-Mahler K, Delattre I, Ducot B, Ferrari P, Bongain A, et al. Cryptorchidism at birth in Nice area (France) is associated with higher prenatal exposure to PCBs and DDE, as assessed by colostrum concentrations. Hum Re prod (2008) 23(8):1708-18. doi:10.1093/humrep/den186
65. McGlynn KA, Guo X, Graubard BI, Brock JW, Klebanoff MA, Longnecker MP. Maternal pregnancy levels of polychlorinated biphenyls and risk of hypospa-dias and cryptorchidism in male offspring. Environ Health Perspect (2009) 117(9):1472-6. doi:10.1289/ehp.0800389
66. Hosie S, Loff S, Witt K, Niessen K, Waag KL. Is there a correlation between organochlorine compounds and undescended testes? Eur J Pediatr Surg (2000) 10(5):304-9.
67. Giordano F, Abballe A, De Felip E, di Domenico A, Ferro F, Grammatico P, et al. Maternal exposures to endocrine disrupting chemicals and hypospa-dias in offspring. Birth Defects Res A Clin Mol Teratol (2010) 88:241-50. doi:10.1002/bdra.20657
68. Carmichael SL, Herring AH, Sjodin A, Jones R, Needham L, Ma C, et al. Hypospadias and halogenated organic pollutant levels in maternal mid-pregnancy serum samples. Chemosphere (2010) 80:641-6. doi:10.1016/j. chemosphere.2010.04.055
69. Damgaard IN, Skakkebaek NE, Toppari J,Virtanen HE, Shen H,Schramm KW, et al. Persistent pesticides in human breast milk and cryptorchidism. Environ Health Perspect (2006) 114:1133-8. doi:10.1289/ehp.8741
70. Fernandez MF, Olmos B, Granada A, Lopez-Espinosa MJ, Molina-Molina JM, Fernandez JM, et al. Human exposure to endocrine-disrupting chemicals and prenatal risk factors for cryptorchidism and hypospadias: a nested case-control study. Environ Health Perspect (2007) 115(1):8-14. doi:10.1289/ ehp.9351
71. Longnecker MP, Klebanoff MA, Brock JW, Zhou H, Gray KA, Needham LL, et al. Maternal serum level of 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene and risk of cryptorchidism, hypospadias, and polythelia among male offspring. Am J Epidemiol (2002) 155:313-22. doi:10.1093/aje/155.4.313
72. Lyche JL, GutlebAC, Bergman A,Eriksen GS, Murk AJ, Ropstad E,et al. Reproductive and developmental toxicity of phthalates. J Toxicol Environ Health B Crit Rev (2009) 12(4):225-49. doi:10.1080/10937400903094091
73. Mylchreest E, Wallace DG, Cattley RC, Foster PMD. Dose-dependent alterations in androgen-regulated male reproductive development in rats exposed to di(n-butyl) phthalate during late gestation. Toxicol Sci (2000) 55:143-51. doi:10.1093/toxsci/55.1.143
74. Parks LG, Ostby JS, Lambright CR,Abbott BD,Klinefelter GR, Barlow NJ,et al. The plasticizer diethylhexyl phthalate induces malformations by decreasing fetal testosterone synthesis during sexual differentiation in the male rat. Toxicol Sci (2000) 58:339-49. doi:10.1093/toxsci/58.2.339
75. WeiderpassE,Adami HO,BaronJA,Wicklund-GlynnA,AuneM,AtumaS,et al. Organochlorines and endometrial cancer risk. Cancer Epidemiol Biomarkers Prev (2000) 9(5):487-93.
76. Ritchie JM, Vial SL, Fuortes LJ, Guo H, Reedy VE, Smith EM. Organochlo-rines and risk of prostate cancer. J Occup Environ Med (2003) 45(7):692-702. doi:10.1097/01.jom.0000071510.96740.0b
77. McGlynn KA, Quraishi SM, Graubard BI, Weber JP, Rubertone MV, Erickson RL. Persistent organochlorine pesticides and risk of testicular germ cell tumors. J Natl Cancer Inst (2008) 100(9):663-71. doi:10.1093/jnci/ djn101
78. Purdue MP, Engel LS, Langseth H, Needham LL, Andersen A, Barr BD, et al. Prediagnostic serum concentrations of organochlorine compounds and risk of testicular germ cell tumors. Environ Health Perspect (2009) 117(10):1514-9. doi:10.1289/ehp.0800359
79. Biggs ML, Davis MD, Eaton DL, Weiss NS, Barr DB, Doody DR, et al. Serum organochlorine pesticide residues and risk of testicular germ cell carcinoma: a population-based case-control study. Cancer Epidemiol Biomarkers Prev (2008) 17:2012-8. doi:10.1158/1055-9965.EPI-08-0032
80. Hardell L,Andersson SO, Carlberg M, Bohr L, van Bavel B, Lindstorm G, et al. Adipose tissue concentrations of persistent organic pollutants and the risk of prostate cancer. J Occup Environ Med (2006) 48:700-7. doi:10.1097/01.jom. 0000205989.46603.43
81. Ritchie JM,Vial SL,Fuortes LJ, Robertson LW,Guo H,ReedyVE,et al. Comparison of proposed frameworks for grouping polychlorinated biphenyl congener data applied to a case-control pilot study of prostate cancer. Environ Res (2005) 98(1):104-13. doi:10.1016/j.envres.2004.05.013
82. Aronson KJ, Wilson JW, Hamel M, Diarsvitri W, Fan W, Woolcott C, et al. Plasma organochlorine levels and prostate cancer risk. J Expo Sci Environ Epidemiol (2009) 20:434-45. doi:10.1038/jes.2009.33
83. Schrader TJ, Langlois I, Soper K, Cherry W. Mutagenicity of bisphenol A (4,4-isopropylidenediphenol) in vitro: effects of nitrosylation. Teratog Carcinog Mutagen (2002) 22:425-41. doi:10.1002/tcm.10039
84. National Toxicology Program. Carcinogenesis bioassay of bisphenol A (CAS no. 80-05-7) in F344 rats and B6C3F mice (feed study). Natl Toxicol Program Tech Rep Ser (1982) 215:1-116.
85. Keri RA, Ho SM, Hunt PA, Knudsen KE, Soto AM, Prins GS. An evaluation of evidence for the carcinogenic activity of bisphenol. Reprod Toxicol (2007) 24:240-52.
86. Ho SM, Tang WY, Belmonte de Frausto J, Prins GS. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogene-sis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res (2006) 66:5624-32. doi:10.1158/0008-5472.CAN-06-0516
87. Naika P, Vijayalaxmib KK. Cytogenetic evaluation for genotoxicity of bisphenol-A in bone marrow cells of Swiss albino mice. Mutat Res (2009) 676:106-12. doi:10.1016/j.mrgentox.2009.04.010
88. Pacchierotti F, Ranaldi R, Eichenlaub-Ritter U, Attia S, Adler ID. Evaluation of a neugenic effects of bisphenol A in somatic and germ cells of the mouse. Mutat Res (2008) 651:64-70. doi:10.1016/j.mrgentox.2007.10.009
89. Amaral Mendes JJ. The endocrine disrupters: a major medical challenge. Food Chem Toxicol (2002) 40(6):781-8. doi:10.1016/S0278-6915(02)00018-2
90. Pan G,Hanaoka T,Yoshimura M,Zhang S,WangP,Tsukino H,et al. Decreased serum free testosterone in workers exposed to high levels of di-n-butyl phtha-late (DBP) and di-2-ethylhexyl phthalate (DEHP): a cross-sectional study in China. Environ Health Perspect (2006) 114(11):1643-8.
91. Duty SM, Calafat AM, Silva MJ, Ryan L, Hauser R. Phthalate exposure and reproductive hormones in adult men. Hum Reprod (2005) 20(3):604-10. doi:10.1093/humrep/deh656
92. Jones HB, Garside DA, Lu R, Roberts JC. The influence of phthalate esters on Leydig cell structure and function in vitro and in vivo. Exp Mol Pathol (1993) 58:179-93. doi:10.1006/exmp.1993.1016
93. Sharpe RM. Hormones and testis development and the possible adverse effects of environmental chemicals. Toxicol Lett (2001) 120:221-32. doi:10.1016/ S0378-4274(01)00298-3
94. Desdoits-LethimonierC,AlbertO,LeBizecB,PerduE,ZalkoD,CourantF,et al. Human testis steroidogenesis is inhibited by phthalates. Hum Reprod (2012) 27:1451-9. doi:10.1093/humrep/des069
95. Foster PM. Mode of action: impaired fetal Leydig cell function - effects on male reproductive development produced by certain phthalate esters. Crit Rev Toxicol (2005) 35:713-9. doi:10.1080/10408440591007395
96. Barlow NJ, Phillips SL,Wallace DG, SarM,Gaido KW, Foster PM. Quantitative changes in gene expression in fetal rat testes following exposure to di(n-butyl) phthalate. Toxicol Sci (2003) 73:431-41. doi:10.1093/toxsci/kfg087
97. Heindel JJ, Powell CJ. Phthalate ester effects on rat Sertoli cell function in vitro: effects of phthalate side chain and age of animal. Toxicol Appl Pharmacol (1992) 115:116-23. doi:10.1016/0041-008X(92)90374-2
98. Clewell RA, Campbell JL, Ross SM, Gaido KW, Clewell HJ III, Andersen ME. Assessing the relevance of in vitro measures of phthalate inhibition of steroido-genesis for in vivo response. Toxicol In vitro (2010) 24:327-34. doi:10.1016/j.tiv.2009.08.003
99. Roelofs MJ, Piersma AH, van den Berg M, van Duursen MB. The rel-evance of chemical interactions with CYP17 enzyme activity: assessment using a novel in vitro assay. Toxicol Appl Pharmacol (2013) 268:309-17. doi:10.1016/j.taap.2013.01.033
100. Dankers AC, Roelofs MJ, Piersma AH, Sweep FC, Russel FG, van den Berg M, et al. Endocrine disruptors differentially target ATP-binding cassette transporters in the blood-testis barrier and affect Leydig cell testosterone secretion in vitro. Toxicol Sci (2013) 136(2):382-91. doi:10.1093/toxsci/kft198
101. DelbesC,LevacherC,Habert R.Estrogen effects onfetal andneonatal testicular development. Reproduction (2006) 132:527-38. doi:10.1530/rep.1.01231
102. Bulger WH, Nuccitelli RM, Kupfer D. Studies on the in vivo and in vitro estrogenic activities of methoxychlor and its metabolites role of hepatic mono-oxygenase in methoxychlor activation.Biochem Pharmacol (1978) 27:2417-23. doi:10.1016/0006-2952(78)90354-4
103. White R, Jobling S, Hoare SA, Sumpter JP, Parker MG. Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology (1994) 135:175-82. doi:10.1210/en.135.1.175
104. Palleschi S, Rossi B, Diana L, Silverstroni L. Di(2-ethylhexyl) phthalate stimulates Ca2+ entry, chemotaxis and ROS production in human granulocytes. Toxicol Lett (2009) 187:52-7. doi:10.1016/j.toxlet.2009.01.031
105. Fong JP, Lee FJ,Lu IS, Uang SN, Lee CC. Estimating the contribution of inhalation exposure to di-2-ethylhexyl phthalate for PCV production workers, suing personal air sampling and urinary metabolite monitoring. Int J Hyg Environ Health (2014) 217(1):102-9. doi:10.1016/j.ijheh.2013.04.002
106. Hulak M, Gazo I, Shaliutina A, Linhartova P. In vitro effects of bisphenol A on the quality parameters, oxidative stress, DNA integrity and adeno-sine triphosphate content in starlet (Acipenser ruthenus) spermatozoa. Comp Biochem Physiol C Toxicol Pharmacol (2013) 158:64-71. doi:10.1016/j.cbpc. 2013.05.002
107. Chitra KC, Latchoumycandane C, Mathur PP. Induction of oxidative stress by bisphenol A in the epididymal sperm of rats. Toxicology (2003) 185:119-27. doi:10.1016/S0300-483X(02)00597-8
108. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet (2002) 3:662-73. doi:10.1038/nrg887
109. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet (2007) 8(4):253-62. doi:10.1038/nrg2045
110. Doshi T, Mehta SS, Dighe V, Balasinor N, Vanage G. Hypermethylation of estrogen receptor promoter region in adult testis of rats exposed neonatally to bisphenol A. Toxicology (2011) 289:74-82. doi:10.1016/j.tox.2011.07.011
111. WuS,ZhuJ,LiY,LinT,GanL,YuanX,et al. Dynamic effectof di-2-(ethylhexyl) phthalate on testicular toxicity: epigenetic changes and their impact on gene expression.IntJ Toxicol (2010)29(2):193-200. doi:10.1177/1091581809355488