Persistent Organochlorine Pollutants with Endocrine Activity and Blood Steroid Hormone Levels in Middle-Aged Men

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Emeville, Elise ^a   Giton, Frank ^b,c   Giusti, Arnaud ^d   Oliva, Alejandro ^e   Fiet, Jean ^c   Thomé, Jean Pierre ^d   Blanchet, Pascal ^a,f   Multigner, Luc ^a  

^a Irset ^*  (Guadeloupe)

^b HENRI MONDOR HOSPITAL   (France)

^c INSERM   (France)

^d UNIVERSITY OF LIÈGE   (Belgium)

^e UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^f Centre Hospitalier Universitaire Guadeloupe   (Guadeloupe)

Author keywords

[No Author keywords available]

Indexed keywords

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; ANDROSTANOLONE; ANDROSTENEDIOL; ANDROSTENEDIONE; CHLORDECONE; ENDOCRINE DISRUPTOR; ESTRADIOL; ESTRONE; ESTRONE SULFATE; FOLLITROPIN; LUTEINIZING HORMONE; ORGANOCHLORINE DERIVATIVE; PERSISTENT ORGANOCHLORINE POLLUTANT; POLYCHLORINATED BIPHENYL; PRASTERONE; PRASTERONE SULFATE; SEX HORMONE BINDING GLOBULIN; STEROID HORMONE; TESTOSTERONE; UNCLASSIFIED DRUG;

ADULT; AGED; ANDROSTENEDIONE BLOOD LEVEL; ARTICLE; ESTRADIOL BLOOD LEVEL; ESTRONE BLOOD LEVEL; FOLLITROPIN BLOOD LEVEL; GUADELOUPE; HUMAN; IMMUNOASSAY; LONG TERM EXPOSURE; LUTEINIZING HORMONE BLOOD LEVEL; MALE; MASS FRAGMENTOGRAPHY; MIDDLE AGED; NORMAL HUMAN; STEROID BLOOD LEVEL; TESTOSTERONE BLOOD LEVEL;

AGED; ENVIRONMENTAL POLLUTANTS; GONADAL STEROID HORMONES; HUMANS; HYDROCARBONS, CHLORINATED; MALE; MIDDLE AGED; PUBLIC HEALTH SURVEILLANCE; RISK FACTORS;

EID: 84879046961     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066460     Document Type: Article

References (58)

1. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, et al. (2009) Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 30: 293-342.
2. Zoeller RT, Brown TR, Doan LL, Gore AC, Skakkebaek NE, et al. (2012) Endocrine-disrupting chemicals and public health protection: a statement of principles from the endocrine society. Endocrinology 153: 4097-4110.
3. Diamanti-Kandarakis E, Palioura E, Kandarakis SA, Koutsilieris M, (2010) The impact of endocrine disruptors on endocrine targets. Horm Metab Res 42: 543-552.
4. Soto AM, Sonnenschein C, (2010) Environmental causes of cancer: endocrine disruptors as carcinogens. Nat Rev Endocrinol 6: 363-370.
5. Danzo BJ, (1997) Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environ Health Perspect 105: 294-301.
6. Ayotte P, Giroux S, Dewailly E, Hernández Avila M, Farias P, et al. (2001) DDT spraying for malaria control and reproductive function in Mexican men. Epidemiology 12: 366-367.
7. Hagmar L, Björk J, Sjödin A, Bergman A, Erfurth EM, (2001) Plasma levels of persistent organohalogens and hormone levels in adult male humans. Arch Environ Health 56: 138-143.
8. Persky V, Turyk M, Anderson HA, Hanrahan LP, Falk C, et al. (2001) The effects of PCB exposure and fish consumption on endogenous hormones. Environ Health Perspect pp. 1275-1283.
9. Martin SA Jr, Harlow SD, Sowers MF, Longnecker MP, Garabrant D, et al. (2002) DDT metabolite and androgens in African-American farmers. Epidemiology 13: 454-458.
10. Richthoff J, Rylander L, Jönsson BA, Akesson H, Hagmar L, et al. (2003) Serum levels of 2,2′,4,4′,5,5′-hexachlorobiphenyl (CB-153) in relation to markers of reproductive function in young males from the general Swedish population. Environ Health Perspect 111: 409-413.
11. Dalvie MA, Myers JE, Lou Thompson M, Dyer S, Robins TG, et al. (2004) The hormonal effects of long-term DDT exposure on malaria vector-control workers in Limpopo Province, South Africa. Environ Res 96: 9-19.
12. Rignell-Hydbom A, Rylander L, Giwercman A, Jönsson BA, Nilsson-Ehle P, et al. (2004) Exposure to CB-153 and p,p′-DDE and male reproductive function. Hum Reprod 19: 2066-2075.
13. Asawasinsopon R, Prapamontol T, Prakobvitayakit O, Vaneesorn Y, Mangklabruks A, et al. (2006) Plasma levels of DDT and their association with reproductive hormones in adult men from northern Thailand. Sci Total Environ 355: 98-105.
14. Giwercman AH, Rignell-Hydbom A, Toft G, Rylander L, Hagmar L, et al. (2006) Reproductive hormone levels in men exposed to persistent organohalogen pollutants: a study of inuit and three European cohorts. Environ Health Perspect 114: 1348-1353.
15. Rylander L, Wallin E, Jönssson BA, Stridsberg M, Erfurth EM, et al. (2006) Associations between CB-153 and p,p′-DDE and hormone levels in serum in middle-aged and elderly men. Chemosphere 65: 375-381.
16. Turyk ME, Anderson HA, Freels S, Chatterton R Jr, Needham LL, et al. (2006) Associations of organochlorines with endogenous hormones in male Great Lakes fish consumers and nonconsumers. Environ Res 102: 299-307.
17. Goncharov A, Rej R, Negoita S, Schymura M, Santiago-Rivera A, et al. (2009) Lower serum testosterone associated with elevated polychlorinated biphenyl concentrations in Native American men. Environ Health Perspect 117: 1454-1460.
18. Langer P, Kocan A, Drobna B, Susienkova K, Radikova Z, et al. (2010) Polychlorinated biphenyls and testosterone: age and congener related correlation approach in heavily exposed males. Endocr Regul 44: 109-114.
19. Haugen TB, Tefre T, Malm G, Jönsson BA, Rylander L, et al. (2011) Differences in serum levels of CB-153 and p,p′-DDE, and reproductive parameters between men living south and north in Norway. Reprod Toxicol 32: 261-267.
20. Blanco-Muñoz J, Lacasaña M, Aguilar-Garduño C, Rodríguez-Barranco M, Bassol S, et al. (2012) Effect of exposure to p,p′-DDE on male hormone profile in Mexican flower growers. Occup Environ Med 69: 5-11.
21. Ferguson KK, Hauser R, Altshul L, Meeker JD, (2012) Serum concentrations of p, p′-DDE, HCB, PCBs and reproductive hormones among men of reproductive age. Reprod Toxicol 34: 429-435.
22. Langer P, Kocan A, Drobna B, Susienkova K, Radikova Z, et al. (2012) Blood testosterone in middle aged males heavily exposed to endocrine disruptors is decreasing more with HCB and p,p′-DDE related to BMI and lipids, but not with Σ15PCBs. Endocr Regul 46: 51-59.
23. Kelce WR, Stone CR, Laws SC, Gray LE, Kemppainen JA, et al. (1995) Persistent DDT metabolite pp′-DDE is a potent androgen antagonist. Nature 376: 581-585.
24. Plísková M, Vondrácek J, Canton RF, Nera J, Kocan A, et al. (2005) Impact of polychlorinated biphenyls contamination on estrogenic activity in human male serum. Environ Health Perspect 113: 1277-1284.
25. Lemaire G, Mnif W, Mauvais P, Balaguer P, Rahmani R, (2006) Activation of alpha- and beta-estrogen receptors by persistent pesticides in reporter cell lines. Life Sci 79: 1160-1169.
26. Hsing AW, Stanczyk FZ, Bélanger A, Schroeder P, Chang L, et al. (2007) Reproducibility of serum sex steroid assays in men by RIA and mass spectrometry. Cancer Epidemiol Biomarkers Prev pp. 1004-1008.
27. Stanczyk FZ, Clarke NJ, (2010) Advantages and challenges of mass spectrometry assays for steroid hormones. J Steroid Biochem Mol Biol 121: 491-495.
28. Multigner L, Ndong JR, Giusti A, Romana M, Delacroix-Maillard H, et al. (2010) Chlordecone exposure and risk of prostate cancer. J Clin Oncol 28: 3457-3462.
29. Giton F, Fiet J, Cornu JN, Cussenot O, Bélanger A, et al. (2011) Serum sex steroids measured in middle-aged European and African-Caribbean men by gas chromatography-mass spectrometry. Eur J Endocrinol 165: 917-924.
30. Giton F, Caron P, Bérubé R, Bélanger A, Barbier O, et al. (2010) Plasma estrone sulfate assay in men: Comparison of radioimmunoassay, mass spectrometry coupled to gas chromatography (GC-MS), and liquid chromatography-tandem mass spectrometry (LC-MS/MS). Clin Chim Acta 411: 1208-1213.
31. Giton F, Urien S, Born C, Tichet J, Guéchot J, et al. (2007) Determination of bioavailable testosterone [non sex hormone binding globulin (SHBG)-bound testosterone] in a population of healthy French men: influence of androstenediol on testosterone binding to SHBG. Clin Chem 53: 2160-2168.
32. Debier C, Pomeroy PP, Dupont C, Joiris C, Comblin V, et al. (2003) Quantitative dynamics of PCB transfer from mother to pup during lactation in UK grey seals Halichoerus grypus. Mar Ecol Prog Ser 247: 237-248.
33. Bernert JT, Turner WE, Patterson DG Jr, Needham LL, (2007) Calculation of serum "total lipid" concentrations for the adjustment of persistent organohalogen toxicant measurements in human samples. Chemosphere 68: 824-831.
34. Jin Y, Hein MJ, Deddens JA, Hines CJ, (2011) Analysis of lognormally distributed exposure data with repeated measures and values below the limit of detection using SAS. Ann Occup Hyg 55: 97-112.
35. Sauerbrei W, Schumacher M, (1992) A bootstrap resampling procedure for model building: application to the Cox regression model. Stat Med 11: 2093-2109.
36. Cohen RA (2009) Classification by Using Stepwise Selection with Validation. In Applications of GLMSELECT Procedure for Megamodel Section. SAS Global Forum. Paper 259-2009, pp 19-22. http://support.sas.com/resources/papers/proceedings09/259-2009.pdf.
37. Centers for Disease Control and Prevention (2009) Fourth Report on Human Exposure to Environmental Chemicals. Atlanta, GA: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention. http://www.cdc.gov/exposurereport/.
38. Dubuisson C, Héraud F, Leblanc JC, Gallotti S, Flamand C, et al. (2007) Impact of subsistence production on the management options to reduce the food exposure of the Martinican population to Chlordecone. Regul Toxicol Pharmacol 49: 5-16.
39. Becker KL (2001) Principles and practice of endocrinology and metabolism. Philadelphia: Lippincott Williams & Wilkins. 957 p.
40. Schmidt KL, Pradhan DS, Shah AH, Charlier TD, Chin EH, et al. (2008) Neurosteroids, immunosteroids, and the Balkanization of endocrinology. Gen Comp Endocrinol 157: 266-274.
41. Owens W, Gray LE, Zeiger E, Walker M, Yamasaki K, et al. (2007) The OECD program to validate the rat Hershberger bioassay to screen compounds for in vivo androgen and antiandrogen responses: phase 2 dose-response studies. Environ Health Perspect 115: 671-678.
42. Kelce WR, Lambright CR, Gray LE Jr, Roberts KP, (1997) Vinclozolin and p,p′-DDE alter androgen-dependent gene expression: in vivo confirmation of an androgen receptor-mediated mechanism. Toxicol Appl Pharmacol 142: 192-200.
43. Lo S, King I, Alléra A, Klingmüller D, (2007) Effects of various pesticides on human 5a-reductase activity in prostate and LNCaP cells. Toxicol in Vitro 21: 502-508.
44. Amory JK, Bremner WJ, (2003) Regulation of testicular function in men: implications for male hormonal contraceptive development. J Steroid Biochem Mol Biol 85: 357-361.
45. Cooke PS, Sato T, Buchanan DL (2001) Disruption of steroid hormone signaling by PCBs. In: Robertson LW, Hansen LG, eds. Recent Advances in Environmental Toxicology and Health effects. Lexington, KY: University press of Kentucky; 257-263.
46. Bonefeld-Jørgensen EC, Andersen HR, Rasmussen TH, Vinggaard AM, (2001) Effect of highly bioaccumulated polychlorinated biphenyl congeners on estrogen and androgen receptor activity. Toxicology 158: 141-153.
47. Oh SM, Ryu BT, Lee SK, Chung KH, (2007) Antiestrogenic potentials of ortho-PCB congeners by single or complex exposure. Arch Pharm Res 30: 199-209.
48. Kester MH, Bulduk S, Tibboel D, Meinl W, Glatt H, et al. (2000) Potent inhibition of estrogen sulfotransferase by hydroxylated PCB metabolites: a novel pathway explaining the estrogenic activity of PCBs. Endocrinology 141: 1897-1900.
49. Machala M, Neca J, Drábek P, Ulrich R, Sabatová V, et al. (1998) Effects of chronic exposure to PCBs on cytochrome P450 systems and steroidogenesis in liver and testis of bulls (Bos taurus). Comp Biochem Physiol A Mol Integr Physiol 120: 65-70.
50. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, et al. (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139: 4252-4263.
51. Thomas P, Dong J, (2006) Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption. J Steroid Biochem Mol Biol 102: 175-179.
52. Benachour N, Moslemi S, Sipahutar H, Seralini GE, (2007) Cytotoxic effects and aromatase inhibition by xenobiotic endocrine disrupters alone and in combination. Toxicol Appl Pharmacol 222: 129-140.
53. Ray S, Xu F, Li P, Sanchez NS, Wang H, et al. (2007) Increased level of cellular Bip critically determines estrogenic potency for a xenoestrogen kepone in the mouse uterus. Endocrinology 148: 4774-4785.
54. Lee J, Scheri RC, Zhang Y, Curtis LR, (2008) Chlordecone, a mixed pregnane X receptor (PXR) and estrogen receptor alpha (ERalpha) agonist, alters cholesterol homeostasis and lipoprotein metabolism in C57BL/6 mice. Toxicol Appl Pharmacol 233: 193-202.
55. Cochran RC, Wiedow MA, (1984) Chlordecone lacks estrogenic properties in the male rat. Toxicol Appl Pharmacol 76: 519-525.
56. Huang ES, Nelson FR, (1986) Anti-estrogenic action of chlordecone in rat pituitary gonadotrophs in vitro. Toxicol Appl Pharmacol 82: 62-69.
57. Multigner L, Kadhel P, Huc-Terki F, Thome JP, Janky E, et al. (2006) Exposure to Chlordecone and Male Fertility in Guadeloupe (French West Indies). Epidemiology 17: S372.
58. Eriksson AL, Lorentzon M, Vandenput L, Labrie F, Lindersson M, et al. (2009) Genetic variations in sex steroid-related genes as predictors of serum estrogen levels in men. J Clin Endocrinol Metab 94: 1033-1041.