Dietary Exposure to Individual Polybrominated Diphenyl Ether

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Article pubs.acs.org/est

Dietary Exposure to Individual Polybrominated Diphenyl Ether Congeners BDE-47 and BDE-99 Alters Innate Immunity and Disease Susceptibility in Juvenile Chinook Salmon Mary R. Arkoosh,*,† Ahna L. Van Gaest,‡ Stacy A. Strickland,‡ Greg P. Hutchinson,‡ Alex B. Krupkin,‡ and Joseph P. Dietrich† †

Environmental & Fisheries Science Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2032 South East OSU Drive, Newport, Oregon 97365, United States ‡ Frank Orth & Associates, Under Contract to Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2032 South East OSU Drive, Newport, Oregon 97365, United States ABSTRACT: Polybrominated diphenyl ethers (PBDEs), used as commercial flame-retardants, are bioaccumulating in threatened Pacific salmon. However, little is known of PBDE effects on critical physiological functions required for optimal health and survival. BDE-47 and BDE-99 are the predominant PBDE congeners found in Chinook salmon collected from the Pacific Northwest. In the present study, both innate immunity (phagocytosis and production of superoxide anion) and pathogen challenge were used to evaluate health and survival in groups of juvenile Chinook salmon exposed orally to either BDE-47 or BDE-99 at environmentally relevant concentrations. Head kidney macrophages from Chinook salmon exposed to BDE-99, but not those exposed to BDE-47, were found to have a reduced ability in vitro to engulf foreign particles. However, both congeners increased the in vitro production of superoxide anion in head kidney macrophages. Salmon exposed to either congener had reduced survival during challenge with the pathogenic marine bacteria Listonella anguillarum. The concentration response curves generated for these end points were nonmonotonic and demonstrated a requirement for using multiple environmentally relevant PBDE concentrations for effect studies. Consequently, predicting risk from toxicity reference values traditionally generated with monotonic concentration responses may underestimate PBDE effect on critical physiological functions required for optimal health and survival in salmon.

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INTRODUCTION Polybrominated diphenyl ethers (PBDEs) are persistent, bioaccumulative, brominated flame-retardants added to household and commercial items that can disassociate from these items and enter the environment. Consequently, PBDEs are found in a number of matrices including air, water, and living species that range from plankton to humans.1−7 PBDE congeners are numbered based upon a system developed for polychlorinated biphenyls.8 The number assigned to the congener reflects the degree of bromination on the aromatic rings. However, environmental samples contain only a small proportion of the 209 possible PBDE congeners in part because of the specific congeners included in the major commercial mixtures and their stability in the environment.9 The three major commercial mixtures (PentaBDE, OctaBDE, and DecaBDE) differ in the amount of higher- or lower-brominated PBDE congeners that comprise the mixtures. The production of PentaBDE and OctaBDE was phased out in the United States in 2004,10 and DecaBDE was voluntarily phased out by U.S. manufacturers in 2013.11 Despite this progress, the potential for exposure to this contaminant will continue for © 2015 American Chemical Society

years because of the continuing use and recycling of products containing the contaminant,12,13 unrestricted use in Asia,11 and existing contamination of the sediment and biota.14 Monitoring studies have determined that outmigrating juvenile Chinook salmon (Oncorhynchus tshawytscha) from Puget Sound and the Columbia River Basin have PBDEs in their whole bodies at concentrations up to 13 000 ng of PBDEs per gram of lipid.5,6,15 Moreover, multiple PBDE congeners were found in the stomach contents and whole bodies of juvenile Chinook salmon at these sites, with the lowerbrominated congeners BDE-47 (2,2′4,4′-tetraBDE) and BDE99 (2,2′4,4′,5-pentaBDE) being the two predominant congeners. The source of lower-brominated PBDE congeners is attributed to the historic use of the commercial mixture PentaBDE that consists primarily of BDE-47 and BDE-99 congeners as well as to the breakdown of higher-brominated Received: Revised: Accepted: Published: 6974

March 2, 2015 April 28, 2015 May 4, 2015 May 4, 2015 DOI: 10.1021/acs.est.5b01076 Environ. Sci. Technol. 2015, 49, 6974−6981

Article

Environmental Science & Technology Table 1. Mean Concentration of Targeted (BDE-47 and BDE-99) and Total PBDEs in the Diets and Whole Bodiesa PBDEs in diets (ng/g of food) diets

BDE-47

BDE-99

total PBDEsb

control

0.4

0.1

0.7

low medium high

32.0 100.0 280.0