Environ. Sci. Technol. 2005, 39, 5612-5619
Polybrominated Diphenyl Ethers and Hydroxylated and Methoxylated Brominated and Chlorinated Analogues in the Plasma of Fish from the Detroit River KARLIS VALTERS,† HONGXIA LI,† MEHRAN ALAEE,‡ IVY D’SA,‡ GO ¨ R A N M A R S H , § , ¶ A° K E B E R G M A N , § A N D R O B E R T J . L E T C H E R * ,† Great Lakes Institute for Environmental Research, University of Windsor, Windsor, Ontario, N9B 3P4 Canada, Aquatic Ecosystem Protection Research Branch, National Water Research Institute, Environment Canada, Burlington, Ontario, L7R 4A6 Canada, and Department of Environmental Chemistry, Stockholm University, SE-106 91 Stockholm, Sweden
Novel classes and congeners of contaminant residues that are structurally analogous to polybrominated diphenyl ether (PBDE) flame retardants were assessed in the plasma of seven benthic- and six pelagic-feeding fish species from the highly contaminated Detroit River corridor, namely, hydroxylated-PBDEs (OH-PBDEs), methoxylatedPBDEs (MeO-PBDEs), and the antimicrobial OH-trichlorodiphenyl ether, triclosan, and its methylated (MeO) triclosan analogue. In all samples ΣPBDE concentrations were comprised mainly of BDE47, BDE99, and BDE100 (>85%) and ranged from 155 pg/g wet weight (ww) to 21 069 pg/g ww. Of the 14 OH-PBDE congeners assessed, as many as 10 congeners were identified, although profiles were generally dominated by 6-OH-BDE47 with lesser amounts of 2′-OH-BDE68, 4′-OH-BDE49, and 4-OH-BDE42. ΣOH-PBDE concentrations ranged from 2.7 to 198 pg/g ww, with ΣPBDE to ΣOH-PBDE concentration ratios ranging from 0.0005 to 0.02. OH-PBDEs are likely derived in these freshwater species as metabolites of precursor PBDEs and are subsequently retained in the blood, for example, 6-OHBDE47, 4′-OH-BDE49, and 4-OH-BDE42 could be derived from BDE47. Portions of concentrations of the OH-PBDEs may also be of alternate origins and are accumulated and retained in these fish. In all samples, the 14 MeO-PBDEs monitored were below detection (10 000 pg/g ww and is clearly a bioaccumulative halogenated phenolic compound in these fish. MeO-triclosan concentrations were considerably lower. In addition to emerging classes of brominated contaminant such as PBDEs, whether of metabolic * Author to whom correspondence should be addressed. Current address: National Wildlife Research Centre, Canadian Wildlife Service, Environment Canada, Raven Road (Carleton University), Ottawa, ON K1A 0H3 Canada; tel.: 613-998-6696; fax: 613-998-0458; e-mail:
[email protected]. † University of Windsor. ‡ National Water Research Institute. § Stockholm University. ¶ Current address: Department of Environmental Chemistry, IIQAB, CSIC, Jordi Girona, 10-18, 08034 Barcelona, Spain. 5612
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or anthropogenic origin, fish collected from the Detroit River are exposed to a complex profile of PBDE-like organohalogens.
Introduction Polybrominated diphenyl ethers (PBDEs) are an important class of additive brominated flame retardants (BFRs) that are now recognized as ubiquitous environmental contaminants (1). North America consumes over half of the world’s production of PBDEs with about 98% of global demand of penta-BDE commercial products. The major congeners in the penta-BDE products, that is, 2,2′,4,4′-tetrabromoDE (BDE47), 2,2′,4,4′,5-pentabromoDE (BDE99), and 2,2′,4,4′,6pentabromoDE (BDE100) (2), are the most widespread in the environment (1, 2). PBDEs have been shown to bioconcentrate in the tissues of fish (3, 4). In wildlife, increasing PBDE concentrations have been found in recent temporal studies on fish and bird tissues from the Great Lakes system. Increasing PBDE levels over the last 20 years or so have been shown in lake trout (Salvelinus namaycush) muscle (5), herring gull (Larus argentatus) eggs (6), and whole body composites of lake trout from Lakes Superior, Michigan, Huron, and Ontario and of walleye (Stizostedion vitreum vitreum) from Lake Erie (7). Structural analogues to PBDEs, mainly tetrabromo- and pentabromo-methoxylated- (MeO)-PBDEs and hydroxylated (OH) PBDEs, have also been detected in blood, and to a lesser extent in adipose and liver tissues of a very limited number of fish, bird, and mammal species from aquatic (marine) environments including the Baltic (8, 9, 10, 11), Atlantic (11, 12), and Arctic (13). In fish specifically, Swedish Atlantic salmon (Salmo salar), herring (Clupea harengus), and commercial fish oils were found to contain a large number of OH-PBDEs and MeO-PBDEs (14, 15). The current thinking is that MeO-PBDEs found in marine wildlife are mostly a consequence of accumulation via natural sources in marine environments (e.g., via formation in sponges and green algae) (10, 12). Despite studies showing that fish are generally slow to depurate higher chlorinated PCB congeners (16), we recently reported OH-PCB metabolites in the blood plasma of Detroit River fish (17). Sum (Σ) OH-PCB concentrations were comparable and for some fish exceeded those of established organohalogen contaminants, for example, ΣPCBs and Σchlordane pesticides (17), which emphasized the potential importance and complexity of halogenated phenolic compound (HPC) exposure in fish from this ecosystem. Residues of OH-PBDEs can be of natural origin or of metabolic derivation likely resulting from cytochrome P450 enzymemediated metabolism of persistent and accumulated precursor PBDEs (14). There are now several recent reports demonstrating that PBDE metabolism via oxidative and debromination pathways occur in fish (18-21). Via oxidative pathways, for example, in northern pike (Esox lucius) dosed with 14C-labeled BDE47, six tetrabromo-OH-PBDE metabolites were detected in several tissues including blood (22). 5-Chloro-2-(2,4-dichlorophenoxy)phenol (triclosan) is a commercially produced and widely used antibacterial and antifungal agent (23, 24). Triclosan is structurally analogous to OH-PBDEs and has been reported as an anthropogenic contaminant in wastewater, surface waters, and aquatic biota (23-25), including waters from the Detroit River (26). Both triclosan and methyl triclosan (MeO-triclosan), 5-chloro-2(2,4-dichlorophenoxy)anisole, are emitted to surface waters 10.1021/es0506410 CCC: $30.25
2005 American Chemical Society Published on Web 07/02/2005
FIGURE 1. A map showing the sampling locations on the Detroit River and study areas (in the insert), where the plasma of 13 fish species was collected. The circled areas in the map are 1, Turkey Creek outlet; 2, River Canard outlet; and 3, Trenton Channel/Celeron Island.
TABLE 1. Species of Pelagic- and Benthic-Feeding Fish Collected from the Detroit River in 2001 and 2002a common name
species
total length (cm)
body weight (g)
N
largemouth bass (L. bass)c,d northern pike (N. pike)b,d white bass (W. bass)b bowfind,e longnose gar (L. gar)b black crappie (B. crappie)b
Pelagic and Piscivorous Micropterus salmoides 30.0-41.0 Esox lucius 38.5-77.0 Morone chrysops 28.5-29.0 Amia calva 51.5-60.0 Lepisosteus osseus 55.5-70.0 Pomoxis nigromaculatus 27.0-27.0
675-1230 292-2800 288-315 1450-1924 296-850 152-289
3 pools of 3 1 pool of 4 1 pool of 3 2 pools of 3 2 pools of 3 1 pool of 2
white sucker (W. sucker)c common carp (C. carp)c,d,e bigmouth buffalo (B. buffalo)e freshwater drum (F. drum)b brown bullhead (B. bullhead)d lake sturgeon (L. sturgeon)f channel catfish (C. catfish)e
Benthic Feeding Catostomus commersoni Cyprinus carpio Ictiobus cyprinellus Aplodinotus grunniens Ameiurus nebulosus Acipenser fulvescens Ictalurus puncyaus
1500-2600 1100-5240 1650-1900 not available 250-567 9150 900
1 pool of 4 5 pools of 3 1 pool of 3 1 pool of 3 2 pools of 4 1 fish only 1 fish only
47.0-60.0 37.4-71.0 36.0-49.0 35-40 18.1-34.2 116.0 48.4
a See the Experimental section for further information. All individuals were collected in areas in the mid to lower part of the Detroit River in the vicinity of Grosse Island at the River Canard outlet, Celeron Island, Trenton Channel, or Turkey Creek outlet (see the map in Figure 1). b River Canard outlet. c Celeron Island. d Trenton Channel. e Turkey Creek outlet. f The single lake sturgeon was collected in Lake St. Clair, i.e., at the inflow of the Detroit River.
via wastewater sewage treatment plants (WSTP) with MeOtriclosan likely being formed by biological methylation in the treatment processes (24, 25). MeO-triclosan can also be an industrial byproduct since triclosan is made from MeOtriclosan (25). OH-PBDEs structurally resemble the thyroid hormone thyroxine (T4) much like OH-PCBs and other HPCs found in blood, and they do this passively as they are retained as residues and thus affect thyroid hormone homeostasis. Like OH-PCBs, some OH-PBDE congeners have been shown to competitively bind with thyroid hormone transport proteins such as transthyretin (TTR) found in mammals and birds (27). Sediment and aquatic biota, including fish from the lower part of the Detroit River, contain high concentrations of persistent polyhalogenated contaminants (e.g., PCBs and DDTs) relative to other areas of the Great Lakes system (16, 28). Recently, PBDEs, mainly comprised of BDE47, were reported in whole body homogenates of largemouth bass and common carp collected in the summer of 1999 from the western branch of the Trenton Channel (29). To our knowledge, there are no present reports on OH-PBDEs or
MeO-PBDEs in freshwater biota from anywhere in the western hemisphere. In the present study, we identify and quantify residue levels of PBDEs, OH-PBDEs, MeO-PBDEs, triclosan, and MeO-triclosan in the blood plasma of 13 fish species collected from the Detroit River. Comparisons are also made to the concentrations of other contaminants, for example, PCBs, OH-PCBs, and OC pesticides (17), to assess the relative importance in terms of exposure to these circulating OH- and MeO-halogenated diphenyl ether contaminants.
Experimental Section Fish Sampling. For 13 species of fish, individuals for each species (1-15) were opportunistically collected in August of 2001 or 2002 from the mid to lower portions of the Detroit River, where high levels of organochlorine contaminants have been reported (Figure 1, Table 1) (17). The fish were captured by gill net, trap net, or electrofishing techniques. Blood was collected from the live fish by cardiac puncture with a 20gauge needle and was placed into 10-mL vacutubes containing sodium heparin as the anticoagulant. The blood samples were immediately separated into plasma and red blood cells VOL. 39, NO. 15, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 2. Concentrations (in pg/g, Wet Weight) of PBDEs, OH-PBDEs, Triclosan, and Methyl Triclosan in Pooled Blood Plasma of Pelagic Fish Species from the Detroit River compound BDE47 BDE99 BDE100 BDE153 BDE154
diphenyl ether substit.
l. bassc
2,2′,4,4′-Br42,2′,4,4′,5-Br52,2′,4,4′,6-Br52,2′,4,4′,5,5′-Br62,2′,4,4′,5,6′-Br6-
5161 2563 940 194 267
695 92 103
