Polyhalogenated aromatic hydrocarbons and metabolites: Relation to circulating thyroid hormone and retinol in nestling bald eagles (Haliaeetus leucocephalus)

Abstract

Polyhalogenated aromatic hydrocarbons are global contaminants that are often considered to be endocrine disruptors and include 1,1-dichloro-2,2-bis(4-chlorophenyl)ethylene (p,p'-DDE), polychlorinated biphenyls (PCBs), and polybrominated diphenyl ethers (PBDEs). The present study examined these compounds and their hydroxylated metabolites or analogues and relationships with circulating thyroid hormones and retinols in plasma from nestling and adult bald eagles in British Columbia, Canada, and California, USA. We also compared our results with published data. Thyroxine (T4) decreased with summation operatorPCB and CB153 in nestling bald eagles, which was congruent with results from nine of 14 other published avian laboratory and field studies. Free thyroid hormone levels also decreased with CB-153 and hydroxylated PCBs (OH-PCBs). Retinol increased with CB118 and CB180 in nestling eagles, decreased with OH-PCBs in a subset of nestlings, and decreased in 7 of 12 PCB published studies. Thyroxine decreased with p,p'-DDE for nestlings and with data reported in one of five other published studies. In our samples, plasma retinol, triiodothyronine (T3), and T4 were independent of summation operatorPBDEs, whereas summation operatorOH-PBDEs were weakly but significantly correlated with increases in T3 and retinol. Adult bald eagles showed no relationship between contaminants and thyroid hormones, which is consistent with other studies of long-lived birds, perhaps because adult birds have time to adjust to contaminant levels. Measurement of circulating thyroid hormones appears to be a more useful biomarker than retinols, given the more consistent response of T4 to PCBs here and reported in the literature. We conclude that current environmental exposures to PCBs in British Columbia and in southern California are associated with significant decreases in T4, suggesting a potential negative effect on the endocrine system of nestling bald eagles.

Effects of polychlorobiphenyls, polybromodiphenylethers, organochlorine pesticides and their metabolites on vitamin A status in lactating grey seals

“…However, although Ellis-Hutchings et al (2006) also observed a significant decrease in vitamin A liver content in DE-71 exposed rats during gestation and lactation, no change in circulating retinol could be detected, suggesting that the mobilisation of vitamin A from the liver was not enhanced. Similarly, no significant correlation between SPBDEs and retinol in blood plasma were found in bald eagles with levels of contamination 10 times higher than the grey seals of the present study (Cesh et al, 2010). On the other hand, American kestrels (Falco sparverius) exposed to environmentally relevant PBDE congener concentrations had lower plasma retinol levels when exposed to BDE-99 and -100, while reduced hepatic retinol and retinyl palmitate concentrations were observed when kestrels were exposed to BDE-47 (Fernie et al, 2005).…”

“…Gabrielsen et al, 2011 reported negative relationships between several HO-PCBs and thyroid hormones in in vivo studies with hooded seals (Cystophora cristata). Similarly, although not demonstrated in wild mammals yet, Cesh et al (2010) found negative correlations between HO-PCBs and retinol in plasma of nestling bald eagle (Haliaeetus leucocephalus). These observations favour a competitive binding of HO-PCBs to TTR in wild animals.…”

“…However, one major concern is likely the demethylation of MeO-PBDEs, which produces OH-PBDEs, a process that has been observed in some fish species (Wan et al, 2009). A competitive binding of HOPBDEs on human TTR has been demonstrated in vitro (Meerts et al, 2000) and negative relationships between SHO-PBDEs and circulating retinol in bald eagles were observed (Cesh et al, 2010). Therefore, the presence of MeO-PBDEs in organisms may have toxicological implications for vitamin A homoeostasis.…”

“…However, PCBs and PBDEs share similar chemical properties and comparable adverse effects have been reported in several marine mammal species (Hall et al, 2003;Beineke et al, 2005;Peden-Adams et al, 2005). Furthermore, an impact of PBDEs on the status of vitamin A has been reported in laboratory animals, as well as in birds (Hallgren et al, 2001;Fernie et al, 2005;Ellis-Hutchings et al, 2006;Cesh et al, 2010). One can therefore assume that PBDEs may also affect vitamin A status in marine mammals.…”

“…Studies on laboratory and wild animals generally report depleted hepatic and adipose tissue retinoid stores as well as increased levels in the kidneys (Zile, 1992;Håkansson et al, 1994;Hallgren et al, 2001;Nyman et al, 2003;Ellis-Hutchings et al, 2006;Mos et al, 2007;Nová k et al, 2008). In plasma, both an increase and a decrease of vitamin A levels have been observed, probably depending on the species, the physiological state and the concentrations at which the animals were exposed (Zile, 1992;Nyman et al, 2003;Nová k et al, 2008;Cesh et al, 2010;Delport et al, 2011).…”