Toxicity of polybrominated diphenyl ethers (de‐71) in chicken (Gallus gallus), mallard (Anas platyrhynchos), and American kestrel (Falco sparverius) embryos and hatchlings

Embryonic survival, pipping and hatching success, and sublethal biochemical, endocrine, and histological endpoints were examined in hatchling chickens (Gallus gallus), mallards (Anas platyrhynchos), and American kestrels (Falco sparverius) following air cell administration of a pentabrominated diphenyl ether (penta‐BDE; DE‐71) mixture (0.01–20 μg/g egg) or poly‐chlorinated biphenyl (PCB) congener 126 (3,3′,4,4′,5‐pentachlorobiphenyl; 0.002 μg/g egg). The penta‐BDE decreased pipping and hatching success at concentrations of 10 and 20 μg/g egg in kestrels but had no effect on survival endpoints in chickens or mallards. Sublethal effects in hatchling chickens included ethoxyresorufin‐O‐dealkylase (EROD) induction and histological changes in the bursa, but these responses were not observed in other species. Polychlorinated biphenyl congener 126 (positive control) reduced survival endpoints in chicken and kestrel embryos and caused sublethal effects (EROD induction, reduced bursal mass and follicle size) in chickens. Mallards were clearly less sensitive than the other species to administered penta‐BDE and PCB 126. In a second experiment, the absorption of penta‐BDE (11.1 μg/g egg, air cell administered during early development) into the contents of chicken and kestrel eggs was determined at various intervals (24 h postinjection, midincubation, and pipping). By pipping, 29% of the penta‐BDE administered dose was present in the egg contents in chickens, and 18% of the administered dose was present in kestrel egg contents. Based on uptake in kestrels, the lowest‐observed‐effect level on pipping and hatching success may be as low as 1.8 μg total penta‐BDE/g egg, which approaches concentrations detected in eggs of free‐ranging birds. Because some penta‐BDE congeners are still increasing in the environment, the toxic effects observed in the present study are cause for concern in wildlife.

[1]  K. Fernie,et al.  Evidence of immunomodulation in nestling American kestrels (Falco sparverius) exposed to environmentally relevant PBDEs. , 2005, Environmental pollution.

[2]  D. Bird,et al.  Changes in reproductive courtship behaviors of adult American kestrels (Falco sparverius) exposed to environmentally relevant levels of the polybrominated diphenyl ether mixture, DE-71. , 2008, Toxicological sciences : an official journal of the Society of Toxicology.

[3]  S. Bursian,et al.  Immunotoxicity of the commercial polybrominated diphenyl ether mixture DE‐71 in ranch mink (Mustela vison) , 2007, Environmental toxicology and chemistry.

[4]  F. Mcnabb,et al.  Avian thyroid development in chemically contaminated environments: is there evidence of alterations in thyroid function and development? , 2003, Evolution & development.

[5]  D. Hoffman,et al.  Comparative developmental toxicity of planar polychlorinated biphenyl congeners in chickens, American kestrels, and common terns , 1998 .

[6]  G. Pendleton,et al.  Developmental toxicity of PCB 126 (3,3',4,4',5-pentachlorobiphenyl) in nestling American kestrels (Falco sparverius). , 1996, Fundamental and applied toxicology : official journal of the Society of Toxicology.

[7]  N. Bunce,et al.  Synthesis of polybrominated diphenyl ethers and their capacity to induce CYP1A by the Ah receptor mediated pathway. , 2001, Environmental science & technology.

[8]  S. Kondrad,et al.  Factors Affecting the Toxicity of Methylmercury Injected into Eggs , 2006, Archives of environmental contamination and toxicology.

[9]  B. Brunström,et al.  Toxicity and 7-ethoxyresorufin O-deethylase-inducing potency of coplanar polychlorinated biphenyls (PCBs) in chick embryos , 2004, Archives of Toxicology.

[10]  D. Henshel,et al.  Environmental Toxicity Studies Using Chickens as Surrogates for Wildlife: Effects of Vehicle Volume , 2005, Archives of environmental contamination and toxicology.

[11]  S. Kondrad,et al.  Species Differences in the Sensitivity of Avian Embryos to Methylmercury , 2009, Archives of environmental contamination and toxicology.

[12]  G. Fox,et al.  Health of Herring Gulls (Larus argentatus) in Relation to Breeding Location in the Early 1990s. II. Cellular and Histopathological Measures , 2007, Journal of toxicology and environmental health. Part A.

[13]  S. Kennedy,et al.  The molecular basis for differential dioxin sensitivity in birds: role of the aryl hydrocarbon receptor. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[14]  M. L. La Guardia,et al.  Polybrominated diphenyl ethers in peregrine falcon (Falco peregrinus) eggs from the northeastern U.S. , 2008, Environmental science & technology.

[15]  F. Mcnabb,et al.  17 – Thyroid Hormone Effects on Growth, Development, and Metabolism , 1993 .

[16]  R. A. McNabb Thyroid Development in Precocial and Altricial Avian Embryos , 1977 .

[17]  A. K. Peters,et al.  Effects of polybrominated diphenyl ethers on basal and TCDD-induced ethoxyresorufin activity and cytochrome P450-1A1 expression in MCF-7, HepG2, and H4IIE cells. , 2004, Toxicological sciences : an official journal of the Society of Toxicology.

[18]  S. Kennedy,et al.  Key amino acids in the aryl hydrocarbon receptor predict dioxin sensitivity in avian species. , 2008, Environmental science & technology.

[19]  D. Alonso,et al.  Coordinate induction of cytochrome P-448 mediated mixed function oxidases and histopathologic changes produced acutely in chick embryo liver by polychlorinated biphenyl congeners. , 1984, Toxicology and applied pharmacology.

[20]  A. K. Peters,et al.  Interactions of polybrominated diphenyl ethers with the aryl hydrocarbon receptor pathway. , 2006, Toxicological sciences : an official journal of the Society of Toxicology.

[21]  K M Crofton,et al.  Effects of short-term in vivo exposure to polybrominated diphenyl ethers on thyroid hormones and hepatic enzyme activities in weanling rats. , 2001, Toxicological sciences : an official journal of the Society of Toxicology.

[22]  F. Mcnabb,et al.  Thyroid development in altricial ring doves, Streptopelia risoria. , 1985, General and comparative endocrinology.

[23]  M. Melancon Development of Cytochromes P450 in Avian Species as a Biomarker for Environmental Contaminant Exposure and Effect: Procedures and Baseline Values , 1996 .

[24]  A. Bosveld,et al.  Occurrence and effects of PCBs, PCDDs and PCDFs in hatchlings of the common tern (Sterna hirundo) , 1993 .

[25]  A Schmoldt,et al.  Induction of rat liver microsomal cytochrome P-450 by the pentabromo diphenyl ether Bromkal 70 and half-lives of its components in the adipose tissue. , 1990, Toxicology.

[26]  V. Darras,et al.  Uptake and tissue‐specific distribution of selected polychlorinated biphenyls in developing chicken embryos , 2005, Environmental toxicology and chemistry.

[27]  T. Kubiak,et al.  PCBs and dioxins in birds , 1996 .

[28]  C. Larsen,et al.  Does thyroid function in developing birds adapt to sustained ammonium perchlorate exposure? , 2004, Toxicological sciences : an official journal of the Society of Toxicology.

[29]  P. S. Pooler,et al.  Ammonium perchlorate effects on thyroid function and growth in bobwhite quail chicks , 2004, Environmental toxicology and chemistry.

[30]  K. Fernie,et al.  Exposure to polybrominated diphenyl ethers (PBDEs): changes in thyroid, vitamin A, glutathione homeostasis, and oxidative stress in American kestrels (Falco sparverius). , 2005, Toxicological sciences : an official journal of the Society of Toxicology.

[31]  P. Darnerud,et al.  Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and chlorinated paraffins (CPs) in rats-testing interactions and mechanisms for thyroid hormone effects. , 2002, Toxicology.

[32]  C. D. de Wit An overview of brominated flame retardants in the environment. , 2002, Chemosphere.

[33]  B. Brunström Sensitivity of embryos from duck, goose, herring gull, and various chicken breeds to 3,3',4,4'-tetrachlorobiphenyl. , 1988, Poultry science.

[34]  D. Tillitt,et al.  Effects of 3,3′,4,4′,5-pentachlorobiphenyl (PCB 126) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) injected into the yolks of chicken (Gallus domesticus) eggs prior to incubation , 1996, Archives of environmental contamination and toxicology.

[35]  E. Jakobsson,et al.  Brominated flame retardants: a novel class of developmental neurotoxicants in our environment? , 2001, Environmental health perspectives.

[36]  D. Bird,et al.  Changes in the Growth, but Not the Survival, of American Kestrels (Falco sparverius) Exposed to Environmentally Relevant Polybrominated Diphenyl Ethers , 2006, Journal of toxicology and environmental health. Part A.

[37]  R C Hale,et al.  Polybrominated diphenyl ether flame retardants in Virginia freshwater fishes (USA). , 2001, Environmental science & technology.

[38]  K. Grasman,et al.  Effects of In Ovo Exposure to PCBs 126 and 77 on Mortality, Deformities and Post-hatch Immune Function in Chickens , 2007, Journal of toxicology and environmental health. Part A.

[39]  Safe,et al.  Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. , 1998, Environmental health perspectives.

[40]  M. DeVito,et al.  Possible mechanisms of thyroid hormone disruption in mice by BDE 47, a major polybrominated diphenyl ether congener. , 2008, Toxicology and applied pharmacology.

[41]  N. Kerkvliet,et al.  Immunologic and endocrine effects of the flame-retardant pentabromodiphenyl ether (DE-71) in C57BL/6J mice. , 1994, Toxicology.

[42]  P. Darnerud,et al.  Effects of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) on thyroid hormone and vitamin A levels in rats and mice , 2001, Archives of Toxicology.

[43]  C. D. de Wit,et al.  Higher brominated diphenyl ethers and hexabromocyclododecane found in eggs of peregrine falcons (Falco peregrinus) breeding in Sweden. , 2004, Environmental science & technology.

[44]  R. Hale,et al.  Contaminant Exposure and Reproductive Success of Ospreys (Pandion haliaetus) Nesting in Chesapeake Bay Regions of Concern , 2004, Archives of environmental contamination and toxicology.

[45]  R. Norstrom,et al.  Geographical distribution (2000) and temporal trends (1981-2000) of brominated diphenyl ethers in Great Lakes hewing gull eggs. , 2002, Environmental science & technology.

[46]  D. Tillitt,et al.  Effect of In Ovo Exposure to an Organochlorine Mixture Extracted from Double Crested Cormorant Eggs (Phalacrocorax auritus) and PCB 126 on Immune Function of Juvenile Chickens , 2007, Archives of environmental contamination and toxicology.

[47]  S. Kennedy,et al.  Role of oxidative stress and antioxidant defense in 3,3',4,4',5-pentachlorobiphenyl-induced toxicity and species-differential sensitivity in chicken and duck embryos. , 2001, Toxicology and applied pharmacology.

[48]  N. Bunce,et al.  Polybrominated diphenyl ethers as Ah receptor agonists and antagonists. , 2003, Toxicological sciences : an official journal of the Society of Toxicology.

[49]  R. Letcher,et al.  Dramatic changes in the temporal trends of polybrominated diphenyl ethers (PBDEs) in herring gull eggs from the Laurentian Great Lakes: 1982-2006. , 2008, Environmental science & technology.

[50]  D. Tillitt,et al.  Relation among cytochrome p450, ah‐active pcb congeners and dioxin equivalents in pipping black‐crowned night‐heron embryos , 1994 .

[51]  B. Brunström,et al.  Differences in sensitivity of some avian species to the embryotoxicity of a PCB, 3,3′,4,4′-tetrachlorobiphenyl, injected into the eggs , 1986 .

[52]  B. Brunström,et al.  EROD induction by environmental contaminants in avian embryo livers. , 1998, Comparative biochemistry and physiology. Part C, Pharmacology, toxicology & endocrinology.

[53]  B. Hull,et al.  Effects of PCB 126 on Primary Immune Organs and Thymocyte Apoptosis in Chicken Embryos , 2005, Journal of toxicology and environmental health. Part A.