Cellular and hormonal disruption of fetal testis development in sheep reared on pasture treated with sewage sludge

Environmental Health Perspectives

Volumn 113, Issue 11, 2005, Pages 1580-1587

  Paul, Catriona ^a   Rhind, Stewart M ^b   Kyle, Carol E ^b   Scott, Hayley ^a   McKinnell, Chris ^a   Sharpe, Richard M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Anti M llerian hormone; Environmental chemicals; Follicle stimulating hormone; FSH; Gonocyte; Inhibin A; Leydig cell; LH; Peritubular myoid cell; Sertoli cell; Sewage sludge; Testosterone

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ANDROGEN RECEPTOR; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); ENVIRONMENTAL CHEMICAL; FOLLITROPIN; INHIBIN A; INORGANIC COMPOUND; LUTEINIZING HORMONE; MUELLERIAN INHIBITING FACTOR; NITROGEN FERTILIZER; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BREEDING; CELL COUNT; CELL VOLUME; CHEMICAL COMPOSITION; CONTROLLED STUDY; CYTOPLASM; EXPERIMENTAL DESIGN; FEMALE; FETUS; FOLLITROPIN BLOOD LEVEL; INTRAUTERINE GROWTH RETARDATION; KIDNEY TUBULE CELL; LEYDIG CELL; LONG TERM EXPOSURE; LUTEINIZING HORMONE BLOOD LEVEL; MALE; NONHUMAN; PASTURE; PRIORITY JOURNAL; SERTOLI CELL; SEX DIFFERENCE; SHEEP; SLUDGE TREATMENT; SOMATIC CELL; TESTIS DEVELOPMENT; TESTIS FUNCTION; TESTIS WEIGHT; TESTOSTERONE BLOOD LEVEL;

ANIMALS; ENVIRONMENTAL POLLUTANTS; FEMALE; FERTILIZERS; FETAL DEVELOPMENT; FOLLICLE STIMULATING HORMONE; INHIBINS; LEYDIG CELLS; LUTEINIZING HORMONE; MALE; MATERNAL EXPOSURE; PREGNANCY; SERTOLI CELLS; SEWAGE; SHEEP; TESTIS; TESTOSTERONE;

ANIMALIA; MYOIDA; OVIS; OVIS ARIES;

EID: 27744598112     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.8028     Document Type: Article

References (56)

1. Akre O, Lipworth L, Cnattinguis S, Sparen P, Ekbom A. 1999. Risk factor patterns for cryptorchidism and hypospadias. Epidemiology 10:364-369.
2. Atanassova NN, Walker M, McKinnell C, Fisher JS, Sharpe RM. 2005. Evidence that androgens and oestrogens, as well as follicle-stimulating hormone, can alter Sertoli cell number in the neonatal rat. J Endocrinol 184:107-117.
3. Bielli A, Perez R, Pedrana G, Milton JT, Lopez A, Blackberry MA, et al. 2002. Low maternal nutrition during pregnancy reduces the number of Sertoli cells in the newborn lamb. Reprod Fertil Dev 14:333-337.
4. Bremner WJ, Millar MR, Sharpe RM, Saunders PTK. 1994. Immunohistochemical localization of androgen receptors in the rat testis: evidence for stage-dependent expression and regulation by androgens. Endocrinology 135:1227-1234.
5. CDC. 2003. Second National Report on Human Exposure to Environmental Chemicals. Publ. No. 02-0716. Atlanta, GA:Centers for Disease Control and Prevention. Available: http://www.cdc.gov/nceh/dls/report/ [accessed 12 May 2003].
6. Cigognani A, Alessandroni R, Pasinin A, Pirazzoli P, Cassio A, Barbieri E, et al. 2002. Low birth weight for gestational age and subsequent male gonadal function. J Pediatr 141:376-380.
7. Commission of the European Communities. 1994. Directorate Generale XI. Waste Management - Sewage Sludge. Part 1. Survey of Sludge Production, Treatment, Quality and Disposal in the European Union. European Commission. Brussels.
8. Corker CS, Davidson DW. 1981. Radioimmunoassay of testosterone in various biological fluids without chromatography. J Steroid Biochem 9:319-323.
9. Da Silva P, Aitken RP, Rhind SM, Racey PA, Wallace JM. 2003. Effect of maternal overnutrition during pregnancy on pituitary gonadotrophin gene expression and gonadal morphology in female and male foetal sheep at day 103 of gestation. Placenta 24:248-257.
10. de Zegher F, Devlieger H, Eeckels R. 1999. Fetal growth: boys before girls. Horm Res 51:258-259.
11. Ewing LL, Zirkin B. 1983. Leydig cell structure and steroidogenic function. Recent Progr Horm Res 39:599-635.
12. Fisher JS, Macpherson S, Marchetti N, Sharpe RM. 2003. Human 'testicular dysgenesis syndrome': a possible model based on in utero exposure of the rat to dibutyl phthalate. Hum Reprod 18:1383-1394.
13. Francois I, de Zegher F, Spiessens C, D'Hooge T, Vanderschueren D. 1997. Low birth weight and subsequent male infertility. Pediatr Res 42:899-901.
14. Gill JW, Hosking BJ. 1995. Acute prenatal androgen treatment increases birth weights and growth rates in lambs. J Anim Sci 73:2600-2608.
15. Great Britain Parliament. 1989. The Sludge (Use in Agriculture) Regulations. Statutory Instruments 1989, No. 1263. London:Her Majesty's Stationary Office.
16. Hindmarsh PC, Geary MP, Rodeck CH, Kingdom JC, Cole TJ. 2002. Intrauterine growth and its relationship to size and shape at birth. Pediatr Res 52:263-268.
17. IPCS (International Programme on Chemical Safety). 2002. Global Assessment of the State-of-the-Science of Endocrine Disruptors (Damstra T, Barlow S, Bergman A, Kavlock R, Van Der Kraak G, eds). Available: http://ehp.niehs.nih.gov/who/ [accessed 12 May 2003].
18. Johnston H, Baker PJ, Abel M, Charlton HM, Jackson G, Fleming L, et al. 2004. Regulation of Sertoli cell number and activity by follicle-stimulating hormone and androgen during postnatal development in the mouse. Endocrinology 145:318-329.
19. A isoform) during the oestrous cycle, after manipulation of ovarian activity and during pregnancy in ewes. J Reprod Fertil 113:159-166.
20. Liao KH, Dobrev ID, Dennison JE Jr, Andersen ME, Reisfeld B, Reardon KF, et al. 2002. Application of biologically based computer modelling to simple or complex mixtures. Environ Health Perspect 110(suppl 6):957-963.
21. Mahood IK, McKinnell C, Fisher JS, Walker M, Hallmark N, Sharpe RM. 2005. Abnormal Leydig cell aggregation in the fetal testis of rats exposed to di(n-butyl) phthalate and its possible role in testicular dysgenesis. Endocrinology 146:613-623.
22. McNeilly AS, Jonassen JA, Fraser HM. 1986. Suppression of follicular development after chronic LHRH immunoneutralization in the ewe. J Reprod Fertil 76:481-490.
23. McNeilly AS, Souza CJ, Baird DT, Swanston IA, McVerry J, Crawford J, et al. 2002. Production of inhibin A not B in rams: changes in plasma inhibin A during testis growth, and expression of inhibin/activin subunit mRNA and protein in adult testis. Reproduction 123:827-835.
24. Mitchell LM, Silveira M, Mylne MJ, Matthews K, Dingwall WS. 2002. Seasonal differences in lamb birthweight do not arise from inherent differences in the oocyte and/or early embryo. Reprod Fertil Dev 14:207-213.
25. Mylchreest E, Sar M, Cattley R, Foster PMD. 1999. Disruption of androgen-regulated male reproductive development by di(n-butyl) phthalate during late gestation in rats is different from flutamide. Toxicol Appl Pharmacol 156:81-95.
26. Olsen J, Bonde J-P, Basso O, Hjollund NHI, Sorensen HT, Abell A. 2000. Birthweight and semen characteristics. Int J Androl 23:230-235.
27. Parks L, Ostby J, Lambright C, Abbott B, Klinefelter GD, Barlow N, et al. 2000. The plasticizer diethylhexyl phthalate induces malformations by decreasing fetal testosterone synthesis during sexual differentiation in the male rat. Toxicol Sci 58:339-349.
28. Rae MT, Kyle CE, Miller DW, Hammond AJ, Brooks AN, Rhind SM. 2002a. The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim Reprod Sci 72:63-71.
29. Rae MT, Rhind SM, Fowler PA, Miller DW, Kyle CE, Brooks AN. 2002b. Effect of maternal undernutrition on fetal testicular steroidogenesis during the CNS androgen-responsive period in male sheep fetuses. Reproduction 124:33-39.
30. Rajapakse N, Silva E, Kortenkamp A. 2002. Combining xenoestrogens at levels below individual no-observed-effect concentrations dramatically enhances steroid hormone action. Environ Health Perspect 110:919-921.
31. Ramaswamy S, Plant TM, Marshall GR. 2000. Pulsatile stimulation with recombinant single chain human luteinizing hormone elicits precocious Sertoli cell proliferation in the juvenile male rhesus monkey (Macaca mulatta). Biol Reprod 63:82-88.
32. Rhind SM, Kyle CE, Own J. 2005a. Accumulation of potentially toxic metals in the liver tissue of sheep grazed on sewage sludge-treated pastures. Anim Sci 81:107-113.
33. Rhind SM, Kyle CE, Telfer G, Duff EI, Smith A. 2005b. Alkyl phenols and diethyl hexyl phthalate (DEHP) in tissues of sheep grazing pastures fertilized with sewage sludge or inorganic fertilizer. Environ Health Perspect 113:447-453.
34. Rhind SM, Rae MT, Brooks AN. 2001. Effects of nutrition and environmental factors on the fetal programming of the reproductive axis. Reproduction 122:205-214.
35. Rhind SM, Smith A, Kyle CE, Telfer G, Martin G, Duff E, et al. 2002. Phthalate and alkyl phenol concentrations in soil following applications of inorganic fertiliser or sewage sludge to pasture and potential rates of ingestion by grazing ruminants. J Environ Monit 4:142-148.
36. Rivas A, Fisher JS, McKinnell C, Atanassova N, Sharpe RM. 2002. Induction of reproductive tract developmental abnormalities in the male rat by lowering androgen production or action in combination with a low dose of diethylstilbestrol: evidence for importance of the androgen-estrogen balance. Endocrinology 143:4797-4808.
37. Schlatt S, Weinbauer G, Arslan M, Nieschlag E. 1993. Appearance of alpha-smooth muscle actin in peritubular cells of monkey testes is induced by androgens, modulated by follicle-stimulating hormone, and maintained after hormonal withdrawal. J Androl 14:340-350.
38. Schwarzler P, Bland JM, Holden D, Campbell S, Ville Y. 2004. Sex-specific antenatal reference growth charts for uncomplicated singleton pregnancies at 15-40 weeks of gestation. Ultrasound Obstet Gynecol 23:23-29.
39. SEDE and Arthur Andersen. 2001. Disposal and Recycling Routes for Sewage Sludge. Part 1. Sludge Use Acceptance Report. European Commission/Directorate Generale Environment. Luxembourg:European Communities.
40. Sharpe RM. 2005. Sertoli cell endocrinology and signal transduction: androgen regulation. In: Sertoli Cell Biology (Griswold M, Skinner M, eds). San Diego:Academic Press, 199-216.
41. Sharpe RM, Irvine DS. 2004. How strong is the evidence of a link between environmental chemicals and adverse effects on human reproductive health? BMJ 328:447-451.
42. Sharpe RM, Skakkebaek NE. 2003. Male reproductive disorders and the role of endocrine disruption: advances in understanding and identification of areas for future research. Pure Appl Chem 75:2023-2038.
43. Sharpe RM, Walker M, Millar MR, Atanassova NN, Morris K, McKinnell C, et al. 2000. Effect of neonatal gonadotropin-releasing hormone antagonist administration on Sertoli cell number and testicular development in the marmoset: comparison with the rat. Biol Reprod 62:1685-1693.
44. Skakkebaek NE, Rajpert-De Meyts E, Main K. 2001. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16:972-978.
45. Smith SR. 1995. Organic pollutants. In: Agricultural Recycling of Sewage Sludge and the Environment. Wallingford, UK:CAB International, 207-236.
46. Swan SH, Elkin EP, Fenster L. 2000. The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ Health Perspect 108:961-966.
47. Swan SH, Main KM, Liu F, Stewart SL, Kruse RL, Calafat AM, et al. 2005. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect 113:1056-1061.
48. Swanson RL, Bortman ML, O'Connor P, Stanford HM. 2004. Science, policy and the management of sewage materials. The New York City experience. Marine Pollut Bull 49:679-687.
49. Sweeney T, Nicol L, Riche JF, Brooks AN. 2000. Maternal exposure to octylphenol suppresses fetal follicle-stimulating hormone secretion, testis size and Sertoli cell number. Endocrinology 141:2667-2673.
50. Tindall H, Ashby J. 2004. Sensitivity of the immature rat uterotrophic assay to mixtures of estrogens. Environ Health Perspect 112:575-582.
51. Toppari J, Larsen JC, Christiansen P, Giwercman A, Grandjean P, Guillette LJ Jr, et al. 1996. Male reproductive health and environmental xenoestrogens. Environ Health Perspect 104(suppl 4):741-803.
52. U.K. Animals (Scientific Procedures) Act. 1986. Available: http://www.homeoffice.go.uk/docs/animallegislation.html.
53. Webber MD, Lesage S. 1989. Organic contaminants in Canadian municipal sludges. Waste Manage Res 7:63-82.
54. Weidner IS, Moller H, Jensen TK, Skakkebaek NE. 1999. Risk factors for crytptorchidism and hypospadias. J Urol 161:1606-1609.
55. Wilkinson JM, Hill J, Livesey CT. 2001. Accumulation of potentially toxic elements in the body tissues of sheep grazed on grassland given repeated applications of sewage sludge. Anim Sci 72:179-190.
56. Zhou ZX, Lane MV, Kemppainen JA, French FS, Wilson EM. 1995. Specificity of ligand-dependent androgen receptor stabilization: receptor domain interactions influence ligand dissociation and receptor stability. Mol Endocrinol 9:208-218.