Statistical Modeling Suggests That Antiandrogens in Effluents from Wastewater Treatment Works Contribute to Widespread Sexual Disruption in Fish Living in English Rivers

By Jobling, Susan; Burn, Robert. W. et al. | Environmental Health Perspectives, May 2009 | Go to article overview

Statistical Modeling Suggests That Antiandrogens in Effluents from Wastewater Treatment Works Contribute to Widespread Sexual Disruption in Fish Living in English Rivers


Jobling, Susan, Burn, Robert. W., Thorpe, Karen, Williams, Richard, Tyler, Charles, Environmental Health Perspectives


BACKGROUND: The widespread occurrence of feminized male fish downstream of some wastewater treatment works has led to substantial interest from ecologists and public health professionals. This concern stems from the view that the effects observed have a parallel in humans, and that both phenomena are caused by exposure to mixtures of contaminants that interfere with reproductive development. The evidence for a "wildlife-human connection" is, however, weak: Testicular dysgenesis syndrome, seen in human males, is most easily reproduced in rodent models by exposure to mixtures of antiandrogenic chemicals. In contrast, the accepted explanation for feminization of wild male fish is that it results mainly from exposure to steroidal estrogens originating primarily from human excretion.

OBJECTIVES: We sought to further explore the hypothesis that endocrine disruption in fish is multicausal, resulting from exposure to mixtures of chemicals with both estrogenic and antiandrogenic properties

METHODS: We used hierarchical generalized linear and generalized linear and generalized additive statistical modeling to explore the associations between modeled concentrations and activities of estrogenic and anti-androgenic chemicals in 30 U.K. rivers and feminized responses seen in wild fish living in these rivers.

RESULTS: In addition to the estrogenic substances, antiandrogenic activity was prevalent in almost all treated sewage effluents tested. Further, the results of the modeling demonstrated that feminizing effects in wild fish could be best modeled as a function of their predicted exposure to both antiandrogens and estrogens or to antiandrogens alone.

CONCLUSION: The results provide a strong argument for a multicausal etiology of widespread feminization of wild fish in U.K. rivers involving contributions from both steroidal estrogens and xenoestrogens and from other (as yet unknown) contaminants with antiandrogenic properties. These results may add further credence to the hypothesis that endocrine-disrupting effects seen in wild fish and in humans are caused by similar combinations of endocrine-disrupting chemical cocktails.

KEYWORDS: antiandrogen, endocrine disruption, estrogen, feminization, fish, testicular dysgenesis. Environ Health Perspect 117:797-802 (2009). doi:10.1289/ehp.0800197 available via http://dx.doi. org/ [Online 7 January 2009]

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Wildlife populations associated with the aquatic environment can be exposed to concentrations of endocrine-disrupting pollutants that are high enough to compromise their reproductive capacity (reviewed by Vos et al. 2000); this exposure may, in turn, have population-level consequences (Kidd et al. 2007). The widespread nature of these abnormalities has led to substantial interest from scientists and the general public. This concern stems, in part, from the hypothesis that reproductive diseases seen in humans are also caused by exposure to the same chemical contaminants (Skakkebaek et al. 2001). However, the actual evidence to support the wildlife--human connection is weak. Moreover, in most cases there is little evidence to link cause and effect in even a single species, let alone multiple species. Some of the best evidence has been found in riverine fish populations where feminization of wild male fish (e.g., Jobling et al. 1998) is thought to be caused predominantly by exposure to steroidal estrogens in wastewater treatment work (WWTW) effluents originating from human and animal excretion (Desbrow et al 1998; Routledge et al. 1998), with minor contributions from other estrogenic chemicals found in WWTWs effluents, such as bisphenols and phthalates, nonylphenols (NPs) and their ethoxylates, and carboxylates (Gibson et al. 2005; Harries et al. 1997; Vajda et al. 2008; Vethaak et al. 2005).

Supporting the role of these steroidal estrogens in the feminization of wild fish, recently, a very strong correlation was shown between the predicted steroidal estrogen content of U. …

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