Dietary Exposure of Juvenile Rainbow Trout (Oncorhynchus mykiss

In this study, juvenile rainbow trout (Oncorhynchus mykiss) held in the laboratory ..... an emerging group of persistent pollutants. Mar. Pollut. Bull...
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Environ. Sci. Technol. 2007, 41, 4913-4918

Dietary Exposure of Juvenile Rainbow Trout (Oncorhynchus mykiss) to 1,2-bis(2,4,6-tribromophenoxy)ethane: Bioaccumulation Parameters, Biochemical Effects, and Metabolism G R E G G T . T O M Y , * ,†,‡ V I N C E P . P A L A C E , †,§ KERRI PLESKACH,† NARGIS ISMAIL,† TYLER OSWALD,† ROBERT DANELL,† KERRY WAUTIER,† AND BOB EVANS† Department of Fisheries and Oceans, Freshwater Institute, Winnipeg, Manitoba R3T 2N6 Canada, Department of Chemistry, University of Manitoba, Winnipeg, Manitoba, R3T 2N6 Canada, and Department of Zoology, University of Manitoba, Winnipeg, Manitoba R3T 2N6 Canada

Juvenile rainbow trout (Oncorhynchus mykiss) were exposed in the laboratory to an environmentally relevant dose of 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE) via their diet for 49 days, followed by 154 days of untreated food to examine bioaccumulation parameters, potential biochemical effects, and metabolic products. There was a linear increase in the amount of BTBPE in fish during the uptake phase of the experiment, and an uptake rate constant of 0.0069 ( 0.0012 (arithmetic mean ( 1 × standard error) nmoles per day was calculated. The elimination of BTBPE from the fish obeyed first-order depuration kinetics (r 2 ) 0.6427, p < 0.001) with a calculated half-life of 54.1 ( 8.5 days. The derived biomagnification factor of 2.3 ( 0.9 suggests that this chemical has a high potential for biomagnification in aquatic food webs. Debrominated and hydroxylated metabolites were not detected in liver extracts and suggest that either biotransformation or storage of BTBPEmetabolites in the hepatic system of fish is minor or that our exposure time frame was too short. Similar concentrations of circulating thyroid hormones, liver deiodinase enzyme activity, and thyroid glandular histology suggest that BTBPE is not a potent thyroid axis disruptor.

Introduction Some chemical members of the family of bromine-based flame retardants (BFRs) are now ubiquitous in the environment. Brominated diphenyl ethers (BDEs), for example, have been detected globally in almost every environmental compartment and their detection has forced industry to phase out production of two formulations: penta and octa-mixtures (1-6). In response to this, the BFR industry has begun to market alternative bromine based compounds to replace the discontinued BDE formulations. One such compound, 1,2bis(2,4,6-tribromophenoxy)ethane (BTBPE), is thought to be replacing the octa-BDE mixture in some commercial ap* Corresponding author e-mail: [email protected]; phone: (204) 983-5167; fax: (204) 984-2403. † Freshwater Institute. ‡ Department of Chemistry, University of Manitoba. § Department of Zoology, University of Manitoba. 10.1021/es070288t CCC: $37.00 Published on Web 06/13/2007

 2007 American Chemical Society

plications. BTBPE is synthesized commercially by the reaction of 1,2-dibromoethane with 2,4,6-tribromophenolate and is used as an additive BFR in acrylonitrile-butadienepolystyrene (ABS) resins and in products such as computers, televisions, and mobile cell phones (7). Annual United States production estimates exceed 450 Mt. In Canada, BTBPE is listed on Canada’s Domestic Substances List (DSL) which has been the subject of review and classification for persistent, bioaccumulative, and toxic compounds (Environmental Defense: www.scorecard.org; Canada’s DSL: www.ec.gc.ca/ substances/ese/eng/dsl/dslprog.cfm). BTBPE has been shown to be one of the major BFRs in electronics recycling facilities (8, 9). More recently, BTBPE has been detected in the atmosphere in the United States and also in biota samples from Lake Winnipeg (Canada) (10, 11). Taken together, these findings clearly suggest that this compound is escaping from products in which it is used. Our ongoing research efforts have focused on increasing our understanding of the impacts that BFRs may pose to the health of fish. In this study, juvenile rainbow trout (Oncorhynchus mykiss) held in the laboratory were exposed to an environmentally relevant concentration (46 ( 2 ng/g, lipid weight) of BTBPE via food for 49 days. A depuration period (154 days) in which fish were fed with untreated food was also included to examine elimination of BTBPE. Bioaccumulation parameters [depuration rate (kd), half-life (t1/2), biomagnification factor (BMF)], metabolites, and thyroid axis (circulating hormone concentrations, hepatic deiodinase enzyme activity, and thyroid gland histology) parameters were determined by analysis of tissue (muscle and liver) and plasma sampled at various time points of the uptake and clearance phases of the experiment.

Materials and Methods Standards and Reagents. Native BTBPE and brominated diphenyl ether (BDE) congeners 71, 126, and 156 (99.9%) were obtained from Wellington Laboratories (Guelph, ON, Canada). Distilled in glass hexane, isooctane, dichloromethane (DCM), and acetone were obtained from Caledon (Edmonton, AB, Canada). Corn oil, gelatin, and tricaine methanesulfonate (MS 222) were purchased from SigmaAldrich (Oakville, ON, Canada). Ottawa sand (20-30 mesh) was obtained from Fisher Scientific (ON, Canada) Food Preparation. Commercial fish food (Martin’s Feed Mills, Elmira, ON, Canada) was placed in a pre-cleaned Hobart blender. Corn oil which was spiked with a known amount of BTBPE (500 µL of 50 ng/µL solution in TMP) was transferred to the blender containing the food. After 20 min of gentle stirring, an aqueous gelatin binder (40 g of gelatin in 1.5 L of H2O) was added. Stirring continued until a firm consistency was observed (∼20 min). The resulting spiked food was air-dried for 40 min, extruded through a 4 mm diameter noodler, thoroughly dried at 10 °C for 48 h, and crushed into pellets. Control food was prepared in the same manner aside from adding the test compounds. Food was stored in the dark at -4 °C to limit the possibility of lightinduced degradation of BTBPE. Using the analytical techniques described below, lipid based concentrations of BTBPE in treated (n ) 4) and untreated (n ) 4) food were determined to be 46.2 ( 2.0 (arithmetic mean ( 1 × standard error) and 0.2 ( 0.1 ng/g, respectively. Average percent lipid in the food was determined to be 13.6 ( 0.5%. Concentrations of BTBPE did not decline in the food from the start of the exposure experiment (day ) 0) to the end of the clearance phase (day ) 203). VOL. 41, NO. 14, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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Experiment. Juvenile rainbow trout (initial mean weights, 202 ( 7 g) were fed spiked food for 49 d, followed by untreated food for 154 d. The daily feeding rate was equal to 1.0% of the mean weight of the fish, adjusted after each sampling period based on the mean weight of the sub-sample of fish that were sacrificed. Feed was presented by sprinkling at the surface of the water and was generally consumed by each group of fish within 1 min. Fifty one (51) fish were used for each treatment and each treatment was held in separate 800 L fiberglass aquaria receiving 1.5 L UV and carbon dechlorinated Winnipeg city tap water/min (12 °C, pH ) 7.9-9.1). The dissolved oxygen was always at a level of saturation. A 12 h light:12 h dark photoperiod was maintained throughout the experiment. Four fish were sampled from each tank on days 0, 7, 14, 28, and 49 of the uptake period and on days 7, 14, 28, 56, 112, and 154 d of the depuration period. Fish were always sampled 24 h after the previous feeding. Sampled fish were euthanized with an overdose (0.8 g/L) of pH buffered MS-222. After fin movement ceased (