Reproduction Symposium: does grazing on biosolids-treated pasture pose a pathophysiological risk associated with increased exposure to endocrine disrupting compounds?

J Anim Sci. 2014 Aug;92(8):3185-98. doi: 10.2527/jas.2014-7763. Epub 2014 Jun 19.

Abstract

Biosolids (processed human sewage sludge), which contain low individual concentrations of an array of contaminants including heavy metals and organic pollutants such as polycyclic aromatic hydrocarbons (PAH), polychlorinated biphenyls (PCB), and polychlorinated dibenzodioxins/polychlorinated dibenzofurans known to cause physiological disturbances, are increasingly being used as an agricultural fertilizer. This could pose a health threat to both humans and domestic and wild animal species. This review summarizes results of a unique model, used to determine the effects of exposure to mixtures of environmentally relevant concentrations of pollutants, in sheep grazed on biosolids-treated pastures. Pasture treatment results in nonsignificant increases in environmental chemical (EC) concentrations in soil. Whereas EC concentrations were increased in some tissues of both ewes and their fetuses, concentrations were low and variable and deemed to pose little risk to consumer health. Investigation of the effects of gestational EC exposure on fetal development has highlighted a number of issues. The results indicate that gestational EC exposure can adversely affect gonadal development (males and females) and that these effects can impact testicular morphology, ovarian follicle numbers and health, and the transcriptome and proteome in adult animals. In addition, EC exposure can be associated with altered expression of GnRH, GnRH receptors, galanin receptors, and kisspeptin mRNA within the hypothalamus and pituitary gland, gonadotroph populations within the pituitary gland, and regional aberrations in thyroid morphology. In most cases, these anatomical and functional differences do not result in altered peripheral hormone concentrations or reproductive function (e.g., lambing rate), indicating physiological compensation under the conditions tested. Physiological compensation is also suggested from studies that indicate that EC effects may be greater when exposure occurs either before or during gestation compared with EC exposure throughout life. With regard to human and animal health, this body of work questions the concept of safe individual concentration of EC when EC exposure typically occurs as complex mixtures. It suggests that developmental EC exposure may affect many different physiological systems, with some sex-specific differences in EC sensitivity, and that EC effects may be masked under favorable physiological conditions.

Keywords: biosolids; endocrine disruption; reproduction; sheep.

Publication types

  • Review

MeSH terms

  • Agriculture / methods*
  • Animals
  • Endocrine Disruptors / analysis
  • Endocrine Disruptors / toxicity*
  • Environmental Exposure*
  • Female
  • Fertilizers / analysis
  • Fertilizers / toxicity*
  • Fetal Development / drug effects*
  • Fetus / metabolism
  • Gonadotropin-Releasing Hormone / metabolism
  • Herbivory / physiology*
  • Humans
  • Hydrocarbons, Aromatic / analysis
  • Hydrocarbons, Aromatic / toxicity
  • Hypothalamus / metabolism
  • Male
  • Ovarian Follicle / drug effects
  • Pituitary Gland / drug effects
  • Sewage / chemistry*
  • Sheep
  • Sheep, Domestic / metabolism*
  • Sheep, Domestic / physiology

Substances

  • Endocrine Disruptors
  • Fertilizers
  • Hydrocarbons, Aromatic
  • Sewage
  • Gonadotropin-Releasing Hormone