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The potential reproductive effects of exposure of domestic ruminants to endocrine disrupting compounds

Published online by Cambridge University Press:  18 August 2016

M.L. Boerjan ,
S. Freijnagel ,
S.M. Rhind  and
G.A.L. Meijer
M.L. Boerjan*
Affiliation:
ID-Lelystad, Institute for Animal Science and Health, PO Box 65, 8200 AB Lelystad, The Netherlands
S. Freijnagel
Affiliation:
ID-Lelystad, Institute for Animal Science and Health, PO Box 65, 8200 AB Lelystad, The Netherlands
S.M. Rhind
Affiliation:
Macaulay Land Use Research Institute, Craigiebuckler AB15 8QH, Aberdeen, UK
G.A.L. Meijer
Affiliation:
ID-Lelystad, Institute for Animal Science and Health, PO Box 65, 8200 AB Lelystad, The Netherlands
*
†E-mail:boerjan@pasreform.com
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Abstract

Chemical compounds that mimic or block some of the actions of the steroid hormone oestradiol, have created public concern primarily because of potential adverse reproductive effects in wildlife and humans. Many studies, in vivo and in vitro, have revealed abnormal reproductive function following exposure to these compounds. The number of chemicals known to have the potential to modulate endocrine functions is increasing. In contrast to humans and wildlife, the potential reproductive effects of exposure of domestic animals to endocrine disrupting compounds (EDC) have been studied little. The aim of this overview is to evaluate the possible contribution of EDC to reproductive failure in domestic ruminants.

Sources and classes of EDC are discussed as well as their structure and the modes of hormone disruption. Endocrine disrupting agents may interfere with the reproductive processes of both males and females at several points of the reproductive cycle and through a range of physiological mechanisms. Extrapolating from the results obtained with laboratory animals, the mechanisms whereby infertility in domestic ruminants might be expressed by exposure to EDC through contaminated food and drinking water are addressed.

A preliminary risk assessment is included and it is concluded that under certain circumstances there may be a significantly enhanced intake of oestrogenic hormones and EDC through sewage-contaminated water or soil-contaminated herbage. The physiological consequences for domestic ruminants of EDC ingestion, at the rates estimated, are largely unknown. However, the levels of exposure to oestrogenic hormones and phthalates in grazing ruminants are such that when studying fertility problems in high-yielding dairy cattle the impacts of exposure to endocrine disruptors via the food and drinking water cannot be neglected.

Keywords

endocrine systemfood contaminationpollutionreproductive disordersruminants
Type
Invited Paper
Information
Animal Science , Volume 74 , Issue 1 , February 2002 , pp. 3 - 12
Copyright
Copyright © British Society of Animal Science 2002

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References

Adams, N. R. 1995. Detection of the effects of phytoestrogens on sheep and cattle. Journal of Animal Science 73: 1509–1515.Google Scholar
Ahel, M., Giger, W. and Koch, M. 1994a. Behaviour of alkylphenol polyethoxylate surfactants in the aquatic environment. I. Occurrence and transformation in sewage treatment. Water Research 28: 1131–1142.CrossRefGoogle Scholar
Ahel, M., Giger, W. and Schaffner, C. 1994b. Behaviour of alkylphenol polyethoxylate surfactants in the aquatic environment. II. Occurrence and transformation in rivers. Water Research 28: 1143–1152.Google Scholar
Ahel, M., Schaffner, C. and Giger, W. 1996. Behaviour of alkylphenol polyethoxylate surfactants in the aquatic environment. III. Occurrence and elimination of their persistent metabolites during infiltration of river water to groundwater. Water Research 30: 37–46.Google Scholar
Arnold, D. L., Bryce, F., McGuire, P. F., Stapley, R., Tanner, J. R., Wrenshall, E., Mes, J., Fernie, S., Tryphonas, H., Hayward, S. and Malcolm, S. 1995. Toxicological consequences of Aroclor 1254 ingestion by female Rhesus (Macaca mulatta) monkeys. 2. Reproduction and infant findings. Food and Chemical Toxicology 33: 457–474.CrossRefGoogle ScholarPubMed
Arnold, S. F., Robinson, M. K., Notides, A. C., Guilette, L. J. J. and McLachlan, J. A. 1996. A yeast oestrogen screen for examining the relative exposure of cells to natural and xenoestrogens. Environmental Health Perspectives 104: 544–548.Google Scholar
Ashfield, L. A., Pottinger, T. G. and Sumpter, J. P. 1998. Exposure of female juvenile rainbow trout to alkylphenolic compounds results in modification to growth and ovosomatic index. Environmental Toxicology 17: 679–686.CrossRefGoogle Scholar
Beard, A. P., Bartelewski, P. M. and Rawlings, N. C. 1999. Endocrine and reproductive function in ewes exposed to the organochlore pesticides lindane or pentachlorophenol. Journal of Toxicology and Environmental Health 56: 23–46.Google Scholar
Belfroid, A. C., Horst, A.van der, Vethaak, A. D., Schäfer, A., Rijs, G. and Cofino, W. P. 1999. Analysis of estrogenic hormones and their glucuronides in surface water and waste water in The Netherlands. Science of the Total Environment 225: 101–108.CrossRefGoogle ScholarPubMed
Belfroid, A. C., Murk, A. J., Voogt, P.de, Schäfer, A. J., Rijs, G. B. J. and Vethaak, A. D. 2000. Endocrine-disrupting compounds in water systems: a pilot study of the occurrence of estrogenic compounds in surface and waste waters in The Netherlands. Riza report no 99·007 (ISBN: 90377952271).Google Scholar
Ben-Jonathan, N. and Steinmetz, R. 1998. Xenoestrogens: the emerging story of bisphenol A. Elsevier Science 9: 124–128.Google Scholar
Boockfor, F. R. and Blake, C. A. 1997. Chronic administration of 4-tert-octylphenol to adult male rats causes shrinkage of the testes and male accessory sex organs, disrupts spermatogenesis, and increases the incidence of sperm deformaties. Biology of Reproduction 57: 267–277.Google Scholar
Carlsen, E., Giwercman, A., Keiding, N. and Skakkebaek, N. E. 1995. Declining semen quality and increasing incidence of testicular cancer: is there a common cause? Environmental Health Perspectives 103: (suppl. 7) 137–139.Google Scholar
Centraal Veevoederbureau in Nederland. 1999. Veevoedertabellen. Central Agency for Animal Feed, Lelystad, The Netherlands.Google Scholar
Colborn, T., Dumanoski, D. and Myers, J. P. 1996. Our stolen future: are we threatening our fertility, intelligence and survival? Abacus, London.Google Scholar
Colborn, T., Saal, A. M.vom and Soto, A. M. 1993. Developmental effects of endocrine disrupting chemicals in wildlife and human. Environmental Health Perspectives 101: 378–384.Google Scholar
Crisp, T. M., Clegg, E. D., Cooper, R. L., Wood, W. P., Anderson, D. G., Baetcke, K. P., Hoffmann, J. L., Morrow, M. S., Rodier, D. J., Schaeffer, J. E., Touart, L. W., Zeeman, M. G. and Patel, Y. M. 1998. Environmental endocrine disruption: an effect assessment and analysis. Environmental Health Perspectives 106: (suppl. 1) 11–56.Google Scholar
Darwash, A. O., Lamming, G. E. and Woolliams, J. A. 1999. The potential for identifying heritable endocrine parameters associated with fertility in post-partum dairy cows. Animal Science 68: 333–347.Google Scholar
Davis, B. J., Maronpot, R. R. and Heindel, J. J. 1994. Di-(2-ethylhexyl)phthalate suppresses estradiol and ovulation in cycling rats. Toxicology and Applied Pharmacology 128: 216–223.Google Scholar
Dechaud, H., Ravard, C., Claustrat, F., Perriere, A. B. de la and Pugeat, M. 1999. Xenoestrogen interaction with human sex hormone-binding globulin (hSHBG). Steroids 64: 328–334.Google Scholar
Diskin, M. G. and Sreenan, J. M. 1986. Progesterone and embryo survival in the cow. In Embryonic mortality in farm animals (ed. Sreenan, J. M. and Diskin, M. G.), pp. 142–158. Martinus Nijhoff, Dordrecht, The Netherlands.Google Scholar
Dodge, J. A. 1998. Structure/activity relationships. Pure and Applied Chemistry 70: 1725–1734.Google Scholar
European Union Commission. 1994. Synoptic document no. 7. Draft of provisional list of monomers and additives used in the manufacture of plastics and coatings intended to come into contact with foodstuffs (updated 15 May 1994). Document CS/ DM/2356. Commission of the European Communities, Directorate-General III, Industry, Industrial Affairs, III: Consumer Goods Industries, Foodstuffs-Legislation and Scientific and Technical Aspects. European Union Commission, Brussels.Google Scholar
Farber, T. M., Arcos, M. and Crawford, L. 1983. Safety evaluation standards in the United States. In Anabolics in animal production. Public health aspects, analytical methods and regulation (ed. Meissonier, E. and Mitchell-Vigneron, J.), pp. 509–514. Soregraph, Paris.Google Scholar
Fries, G. F. 1981. Potential polychlorinated biphenyl residues in animal products from application of contaminated sewage sludge to land. Journal of Environmental Quality 11: 14–20.Google Scholar
Giger, W., Brunner, P. H. and Schaffner, C. 1984. 4-Nonylphenol in sewage sludge: accumulation of toxic metabolites from nonionic surfactants. Science 225: 623–625.Google Scholar
Hafne, A. L., Byskov, A. G., Larsen, C. Y. and Tverdan, A. 2000. Reponse on spontaneous and induced maturation in vitro from estradiol, diethylstilbestrol and octylphenol in mouse oocytes. Theriogenology 53: 454 (abstr. ).Google Scholar
Harris, C. A., Henttu, P., Parker, M. G. and Sumpter, J. P. 1997. The oestrogenic activity of phthalate esters in vitro . Environmental Health Perspectives 105: 802–811.Google Scholar
Healy, W. B. 1967. Ingestion of soil by sheep. Proceedings of the New Zealand Society of Animal Production 27: 109–120.Google Scholar
Healy, W. B. 1968. Ingestion of soil by dairy cows. New Zealand Journal of Agricultural Research 11: 487–499.Google Scholar
Helleday, T., Tuominen, K.-L., Bergman, A. and Jenssen, D. 1999. Brominated flame retardants induce intragenic recombination in mammalian cells. Mutation Research 439: 137–147.Google Scholar
Howdeshell, K. L., Hotchkiss, A. K., Thayer, K. A., Vandenbergh, J. G. and vom Saal, F. S. 1999. Exposure to bisphenol A advances puberty. Nature 401: 763–764.Google Scholar
Hoyer, P. B. 1999. Ovotoxic environmental chemicals: indirect endocrine disruptors. In Endocrine disruptors: effects on male and female reproductive systems (ed. Naz, R. K.), pp. 57–124. CRC Press, Boca Raton.Google Scholar
Hyder, S. M., Kirkland, J. L., Loose-Mitchell, D.S, Makela, S. and Stancel, G. M. 1999. Differential regulation of gene expression by oestrogenic ligands: a potential basis for the toxicity of environmental oestrogens. In Endocrine disruptors: effects on male and female reproductive systems (ed. Naz, R. K.), pp. 165–186. CRC Press, Boca Raton.Google Scholar
Jager, D. T. and Visser, C. J. M. 1999. Uniform system for the evaluation of substances, version 3.0. RIVM report no. 601450004.Google Scholar
Jobling, S., Reynolds, T., White, R., Parker, M. G. and Sumpter, J. P. 1995. A variety of environmentally persistent chemicals, including some phthalate plasticizers, are weakly estrogenic. Environmental Health Perspectives 103: 582–587.Google Scholar
Kelce, W. R., Gray, L. E. and Wilson, E. M. 1998. Anti-androgens as environmental endocrine disruptors. Reproduction, Fertility and Development 10: 105–111.Google Scholar
Koopman-Esseboom, C., Morse, D. C., Weisglas-Kuperus, N., Lutkeschipholt, I. J., Paauw, C. G.van der, Tuinstra, L. G. M. T., Brouwer, A. and Sauer, P. J. J. 1994. Effects of dioxins and polychlorinated biphenyls on thyroid hormone status of pregnant women and their infants. Pediatric Research 36: 468–473.Google Scholar
Krishnan, A. V., Stathis, P., Permuth, S. F., Tokes, L. and Feldman, D. 1993. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132: 2279–2286.Google Scholar
Liehr, J. G., Somasunderam, A. and Roy, D. 1998. Natural and anthropogenic environmental oestrogens: the scientific basis for risk assessment. Pure and Applied Chemistry 70: 1747–1758.Google Scholar
McLachlan, J. A. and Arnold, S. F. 1996. Environmental estrogens. American Scientist 84: 452–461.Google Scholar
Majdic, G. and Saunders, P. T. K. 1998. Altered gene expression in the foetal rat testis following the oestrogen exposure. Acta Chimica Slovenica 45: 59–67.Google Scholar
Meijer, G. A. L., Bree, J. A.de, Wagenaar, J. A. and Spoelstra, S. F. 1999. Sewerage overflows put production and fertility of dairy cows at risk. Journal of Environmental Quality 28: 1381–1383.Google Scholar
Ministry of Agriculture, Fisheries and Food. 1987. Survey of plasticiser levels in food contact materials and in foods. Food surveillance paper no. 21. Her Majesty’s Stationery Office, London.Google Scholar
Mirocha, C. J., Pathre, S. V., Schauerhamer, B. and Christensen, C. M. 1976. Natural occurence of fusarium toxins in feedstuff. Applied and Environmental Microbiology 32: 553–556.CrossRefGoogle ScholarPubMed
Morse, D. C., Groen, D., Veerman, M., Amerongen, C. J. van, Koeter, H. B. W. M., Smits-van-Prooije, A.E., Visser, T. J., Koeman, J. H. and Brouwer, A. 1993. Interference of polychlorinated biphenyls in hepatic and brain thyroid hormone metabolism in fetal and neonatal rats. Toxicology and Applied Pharmacology 122: 27–33.Google Scholar
Müller, S. and Schlatter, C. 1998. Natural and antropogenic environmental oestrogens: the scientific basis for risk assessment. Oestrogenic potency of nonylphenol in vivo — a case study to evaluate the relevance of human non-occupational exposure. Pure and Applied Chemistry 70: 1847–1853.Google Scholar
Nakai, M., Tabira, Y., Asai, D., Yakabe, Y., Shimyozu, T., Noguchi, M., Takatsuki, M. and Shimohigashi, Y. 1999. Binding characteristics of dialkyl phthalates for the estrogen receptor. Biochemical and Biophysical Research Communications 254: 311–314.Google Scholar
Naz, R. K. 1999. Endocrine disruptors: effects on male and female reproductive systems. CRC Press, Boca Raton.Google Scholar
Newbold, R. R. 1999. Diethylstilbestrol (DES) and environmental estrogens influence the developing female reproductive system. In Endocrine disruptors: effects on male and female reproductive systems (ed. Naz, R. K.), pp. 39–56. CRC Press, Boca Raton.Google Scholar
Nimrod, A. C. and Benson, W. H. 1996. Environmental estrogenic effects of alkylphenol ethoxylates. Critical Reviews in Toxicology 26: 335–364.Google Scholar
O’Connor, G.A., Chaney, R. L. and Ryan, J. A. 1991. Bioavailability to plants of sludge-borne toxic organics. Reviews of Environmental Contamination and Toxicology 121: 129–155.Google Scholar
Perry, J. S., Heap, R. B., Burton, R. D. and Gadsby, J. E. 1976. Endocrinology of the blastocyst and its role in the establishment of pregnancy. Journal of Reproduction and Fertility, Supplement 25: 85–104.Google Scholar
Pocar, P., Brevini-Gandolfi, T. A. L., Navarette Santos, A., Perazolli, F., Cillo, F., Lauria, A., Fischer, B. and Gandolfi, F. 2000. Mechanisms of PCBs toxicity during in vitro maturation of bovine oocytes. Theriogenology 53: 465 (abstr.).Google Scholar
Pritchard, J. Y., Schrick, F. N. and Inskeep, E. K. 1994. Relationship of pregnancy rate to peripheral concentrations of progesterone and estradiol in beef cows. Theriogenology 42: 247–259.Google Scholar
Pusateri, A. P., Rothschild, M. F., Warner, C. M. and Ford, S. P. 1990. Changes in morphology, cell number, cell size and cellular estrogen content of individual littermate pig conceptuses on days 9 and 13 of gestation. Journal of Animal Science 68: 3727–3735.Google Scholar
Roos, A. H., Berende, P. L. M., Rhijn, J. A.van, Traag, W. A., Mengelers, M. J. B. and Tuinstra, L. G. M. Th. 1991. [Excretion of polychlorinated dibenzo-p-dioxins and –furans in milk of cows fed on dioxins in the dry period.] RIKILT report no. 91.01.Google Scholar
Setchell, B. 1997. Sperm counts in semen of farm animals 1932-1995. International Journal of Andrology 20: 209–214.Google Scholar
Sharman, M., Read, W. A., Castle, L. and Gilbert, L. 1994. Levels of di-(ethylhexyl)phthalate and total phthalate esters in milk, cream, butter and cheese. Food Additives and Contaminants 11: 375–385.Google Scholar
Sharpe, R. M., Fisher, J. S., Millar, M. M., Jobling, S. and Sumpter, J. P. 1995. Gestational and/or neonatal exposure of rats to environmental oestrogenic chemicals results in reduced testicular size and sperm counts in adult life. Environmental Health Perspectives 103: 1136–1143.Google Scholar
Sheenan, D. M. and Young, M. 1979. Diethylstilbestrol and estradiol binding to serum albumin and pregnancy plasma of rat and human. Endocrinology 104: 1442–1446.Google Scholar
Smith, S. R. 1995. Agricultural recycling of sewage sludge and the environment. CAB International, Wallingford.Google Scholar
Sweeney, T., Nicol, L., Roche, J. F. and Brooks, A. N. 2000. Maternal exposure to octylphenol suppresses ovine fetal follicle hormone secretion, testis size, and sertoli cell number. Endocrinology 141: 2667–2673.Google Scholar
Thomas, K. B. and Colborn, T. 1992. Organochlorine endocrine disruptors in human tissue. In Chemically-induced alteration in sexual and functional development: the wildlife/ human connection (ed. Colborn, T. and Clement, T.) Advances in Modelling Environmental Toxicology vol. 21, pp. 365–394.Google Scholar
Toppari, J., Larsen, J., Christiansen, P., Giwercman, A., Grandjean, P., Guilette, L. J., Keiding, N., Leffers, H., Mclachlan, J. A., Meyer, O., Müller, J., Rajpert-De Meyts, E., Scheike, T., Sharpe, R., Sumpter, J. and Skakkebaek, N. E. 1996. Male reproductive health and environmental xenoestrogens. Environmental Health Perspectives 104: (suppl. 4) 741–803.Google Scholar
Velle, W. 1983. Endogenous anabolic agents in farm animals. In Anabolics in animal production. Public health aspects, analytical methods and regulation (ed. Meissonier, E. and Mitchell-Vigneron, J.), pp. 509–514. Soregraph, Paris.Google Scholar
Watkins, J. B. and Klaassen, C. D. 1986. Xenobiotic biotransformation in livestock: comparison to other species commonly used in toxicity testing. Journal of Animal Science 63: 933–942.Google Scholar
Weber, M. D. and Lesage, S. 1989. Organic contaminants in Canadian municipal sludges. Waste Management and Research 7: 63–82.CrossRefGoogle Scholar
White, R., Jobling, S., Hoare, S. A., Sumpter, J. P. and Parker, M. G. 1994. Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology 135: 175–182.Google Scholar
Wild, S. R. and Jones, K. C. 1992. Organic chemicals entering agricultural soils in sewage sludges: screening for their potential to transfer to crop plants and livestock. Science of the Total Environment 119: 85–119.Google Scholar
Wojtowicz, A. K., Gregoraszczuk, E. L., Lyche, J. L. and Ropstad, E. 1999. Effects of in vitro treatment of nondioxin-like (PCB153) and dioxin-like (PCB126) polychlorinated biphenyl on follicular cells steroidogenesis. Proceedings of the third conference of the European Society for Domestic Animal Reproduction, p. 95 (abstr. ).Google Scholar