Environ. Sci. Technol. 2008, 42, 6755–6761
Assessment of Polybrominated Diphenyl Ether Exposures and Health Risks Associated with Consumption of Southern Mississippi Catfish D A N I E L E F . S T A S K A L , * ,† LAURA L.F. SCOTT,‡ LAURIE C. HAWS,† WILLIAM J. LUKSEMBURG,§ LINDA S. BIRNBAUM,| JON D. URBAN,† E. SPENCER WILLIAMS,‡ DENNIS J. PAUSTENBACH,⊥ AND MARK A. HARRIS‡ ChemRisk, Austin, Texas, ChemRisk, Houston, Texas, Vista Analytical Laboratory, El Dorado Hills, California, U.S. Environmental Protection Agency, Research Triangle Park, North Carolina, and ChemRisk, San Francisco, California
Received April 3, 2008. Revised manuscript received May 19, 2008. Accepted June 12, 2008.
Despite the growing public interest in polybrominated diphenyl ethers (PBDEs), there are relatively few studies in the published literature which characterize and quantify human intake of these compounds. In this study, PBDE concentrations were measured in southern Mississippi catfish to determine background levels, daily intake, and risk associated with the consumption of these chemicals from a primary food source for residents in this region of the United States. A total of 33 wild catfish samples were collected from five sites, and 28 farmraised catfish samples were purchased, all of which were from locations in southern Mississippi. All samples were analyzed for 43 PBDEs (mono- through deca-congeners) using highresolution gas chromatography-mass spectrometry. Both PBDE concentrations (∑PBDE ranged from 0.3 to 23.3 ng/g wet weight) and congener profiles varied by fish type and location; however, BDE congeners 47, 99, 100, 153, and 154 were the dominant contributors in all samples. The estimated daily intake of PBDEs associated with consumption of the catfish ranged from 0.03 to 1.80 ng/kg-day. Evaluation of the cancer risk for BDE 209 and the noncancer hazard for BDE congeners 47, 99, 153, and 209 indicated that health risks/hazards due to fish consumption in adults are substantially lower than risk levels generally considered to be at the U.S. EPA minimum concern level.
Introduction Polybrominated diphenyl ethers (PBDEs) are a group of halogenated compounds that include 209 different congeners which vary in both number and position of the bromine atoms. This group of chemicals has been used in a wide variety of consumer products, such as electronic equipment, * Corresponding author phone: (512) 382-5285; fax: (512) 3826945; e-mail:
[email protected]. † ChemRisk, Austin. ‡ ChemRisk, Houston. § Vista Analytical Laboratory. | U.S. Environmental Protection Agency. ⊥ ChemRisk, San Francisco. 10.1021/es800613k CCC: $40.75
Published on Web 07/30/2008
2008 American Chemical Society
upholstered furniture, and polyurethane foams, to increase their resistance to fire (1). However, the actual number of PBDE congeners used in the commercial products (PentaBDE, OctaBDE, and DecaBDE mixtures) was less than the theoretical number of congeners, which is primarily due to the production process and relative stability of the individual congeners (1, 2). Despite differences in the commercial usage patterns of PBDE mixtures, the lower brominated congeners (e.g., tetra- and penta-substituted congeners) are generally found at higher levels than the nona- and decabrominated congeners in humans (3–5). More recently, it has been demonstrated that PBDE congener profiles in environmental media and human biota include BDEs 47, 99, 100, 153, and 154 as well as 209 (3–7). The general lack of consistency between PBDE congener patterns observed in the environment and human tissue and the commercial mixtures most commonly used may be a function of the physical and chemical properties of these compounds, which results in differences in metabolic capacity or environmental fate and transport. Commercial production of PBDEs began in the 1970s (8), and reports of their presence in the environment began surfacing in the early 1980s. However, concerns about PBDEs have increased in recent years as a result of evidence indicating their ability to produce adverse effects in experimental studies along with the finding that they are ubiquitous in the environment and human tissues (2). To date, human exposures to PBDEs have not yet been fully characterized, although exposures via dust and dietary intake are two pathways that have been the focus of attention (9, 10). Recent estimates suggest that dust exposure is the predominant pathway (9, 11); however, because of their structural similarity to other persistent halogenated compounds, dietary exposure has also been considered a predominant exposure route for PBDEs. As such, several investigators have measured levels of PBDEs in common food products (12–18); yet, only a few studies characterize dietary exposure of the U.S. population. Schecter and colleagues (17, 19, 20) conducted a series of analyses to evaluate levels of PBDEs in a variety of food items in the U.S. (mainly in Texas). The authors’ findings indicated that fish products generally contained higher levels of PBDEs than other food products (17, 19, 20). In addition, when these findings were compared to studies conducted in other parts of the world, the results suggested that the levels of PBDEs in food products vary by geographic region. Given these regional differences in the concentrations of PBDEs in food products, characterization of human exposure to these compounds via dietary intake should ideally be based on region-specific data. As such, the objective of this study was to quantify tissue levels of PBDEs in wild-caught and farm-raised catfish collected throughout southern Mississippi. Given that catfish have traditionally been a common staple in the diet of individuals living in this region of the U.S., this food source may significantly contribute to the intake of PBDEs for people living in this region. To characterize exposure and potential health risk, measured PBDE concentrations were then used to estimate dietary intake and to evaluate, for some congeners, risk associated with catfish consumption.
Materials and Methods Sample Collection. A total of 61 wild-caught and farm-raised catfish samples from southern Mississippi were collected in March 2006. Detailed collection procedures have been described previously (21, 22). Briefly, 28 farm-raised catfish samples were purchased from farms or local grocery/seafood VOL. 42, NO. 17, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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markets throughout southern Mississippi. Farm-raised catfish were either purchased as fillets, dressed samples (whole fish with no head or skin), or nuggets (small pieces of fish which may be cut from regular blocks or blocks of minced fish). A total of 33 wild catfish were collected along the Mississippi (one location), Pearl (two locations), and Leaf (two locations) Rivers. Because sampling relied on obtaining fish directly from local anglers, these locations were selected on the basis of identification of popular fishing areas where residents caught fish for consumption. The number of fish collected at each location was dependent on the number of fish local anglers were able to catch within a three to four hour time frame. Although sampling focused on obtaining the edible portion of fish (i.e., fillets), sampling team discussions with local anglers/residents at the second location on the Leaf River revealed that “fingerling” (i.e. small, whole fish) were often eaten intact. As such, several samples of these fish were collected from this site and analyzed on a “whole fish” basis. All other wild-caught catfish were filleted prior to analysis as described by Scott et al. (21). Each sample was measured for length and weighed, and final fillet weights were recorded for filleted fish. Tissue Analysis. Fish tissue samples were analyzed by Vista Analytical Laboratory (El Dorado Hills, CA) for 43 PBDEs ranging from the monobrominated congeners through the fully brominated BDE (IUPAC congener numbers 1, 2, 3, 7, 8, 10, 11, 12, 13, 15, 17, 25, 28, 32, 33, 35, 37, 30, 47, 49, 66, 71, 75, 77, 85, 99, 100, 116, 119, 126, 138, 153, 154, 155, 156, 166, 181, 183, 190, 197, 203, 207, and 209) using highresolution gas chromatography-mass spectrometry using EPA method 1614. BDEs 8 and 11, 12 and 13, and 28 and 33 coeluted; each coeluting pair was reported as a single concentration (i.e., reported as BDE 8/11, 12/13, and 28/33). Nondetect concentrations were assumed to have a concentration equal to the limit of detection (LOD) divided by the square root of 2 (23). The impact of using ND ) LOD/2 versus ND ) 0 is addressed in the Supporting Information (lower concentrations were achieved when ND ) 0); however, for the purposes of this manuscript, the more conservative approach (ND ) LOD/2) was utilized. Data Analysis. Total PBDE concentration was calculated for each sample by summing each congener’s wet weight concentration. All concentrations are presented in nanograms per gram (ppb) of wet weight; however, some lipid-adjusted values are provided. In addition, individual fish data are provided in the Supporting Information. The arithmetic mean, median, and range of ∑PBDEs were characterized by fish type (wild-caught and farm-raised), sample type (fillet, whole, nugget, and dressed), and collection site. Differences between and among groups were examined using the Wilcoxon rank sum test (Kruskal-Wallis test for comparing more than two groups). Because multiple comparisons were made simultaneously, the critical R value (R ) 0.05) was adjusted using the Bonferroni correction. Estimated Daily Intake and Risk Evaluation. The daily intake of all measured PBDEs; the hazard index for BDEs 47, 99, 153, and 209; and the theoretical cancer risk associated with consumption of BDE 209 were calculated using eqs 1, 2, and 3, respectively. Daily Intake ) (C × IR × EF × ED) ⁄ (BW × AT) Hazard Index )
(1)
∑ PBDE Congener Hazard Quotients ) ∑ (Daily Intake) ⁄ (RfD) (2)
Cancer Risk (BDE 209 only) ) (C × IR × CF × EF × ED × CSF) ⁄ (BW × AT) (3) For eqs 1 and 3, C is the mean ∑PBDE wet weight concentration for all fish, and IR is the mean or 95th percentile 6756
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daily fish ingestion rate (3.6 and 21.7 g/day, respectively) based on freshwater finfish consumption rates for the general United States population (Table 10-7 in ref 24). It should be noted that these ingestion rates are believed to be conservative estimates given that the mean ingestion rate is between the 90th and 95th percentile values. Additionally, these ingestion rates are based on the consumption of all types of freshwater finfish rather than just catfish alone. Exposure frequency (EF) was assumed to be 365 days/year; exposure duration (ED) was assumed to be 30 years, and body weight (BW) was assumed to be 70 kg. For daily intake estimates, averaging time (AT) was assumed to be 10,950 days (EF × ED). Daily intake estimates are reported as nanograms of PBDE per kilogram of body weight per day based on measured wet weight concentrations. For eq 2, the hazard quotients for BDEs 47, 99, 153, and 209 were calculated using reference dose (RfD) values as reported in the draft U.S. EPA IRIS Toxicological Evaluations (25–28). The draft RfD value was 0.1 µg/kg-day for both BDEs 47 and 99, 0.2 µg/kg-day for BDE 153, and 7 µg/kg-day for BDE 209. To estimate the theoretical cancer risk for BDE 209 (eq 3), an AT of 25,550 days (70 years × 365 days/year) was used along with a conversion factor (CF) of 1 × 10-3. Finally, the oral cancer slope factor (CSF) for BDE 209 of 7 × 10-4 mg/kg-day-1 as proposed in the draft U.S. EPA IRIS Toxicological Evaluation (28) was utilized in the risk calculation.
Results Several different types of wild-caught catfish were collected, including blue (n ) 17), flathead (n ) 3), and channel (n ) 13) catfish (fish characteristics by fish/sample type and collection location are presented in the Supporting Information). The median fish weight for wild-caught fish later filleted (16.5 ounces) was almost 10 times that for fish analyzed whole (1.8 ounces, all nine whole fish were collected at the Leaf River 2 location). A similar trend was observed for fish length; however, the median length of filleted wild-caught fish was only twice that of whole wild-caught fish. The farm-raised samples had a considerably higher mean lipid fraction than wild-caught samples (8.2% vs 1.5%, respectively). The median ∑PBDE concentration in all samples was 0.9 ng/g wet weight (119.7 ng/g lipid weight (lw)) and ranged from 0.3 to 23.3 ng/g wet weight (3.6 to 4731.9 ng/g lw). Wild-caught catfish had significantly higher levels of ∑PBDE than farmed catfish (p < 0.01) and also had a wider range of levels (Table 1A). Wild-caught catfish fillets had a median concentration of 2.7 ng/g wet weight (227.1 ng/g lw), whereas farm-raised catfish fillets had a median ∑PBDE concentration of 0.5 ng/g wet weight (5.8 ng/g lw). Wild-caught whole fish, which were the smallest fish collected, generally had the highest concentrations of ∑PBDE. The median PBDE concentration in these fish was 10.6 ng/g wet weight (1670.4 ng/g lw). PBDE concentrations in wild-caught catfish varied significantly by sampling location (p < 0.01; Table 1B). Levels of PBDEs in catfish collected in the Pearl River and Ross Barnett Spillway (both of which were locations along the Pearl River) were significantly different (p ) 0.01) when evaluated on a wet weight basis, but not when levels were normalized for lipid content. Levels of PBDEs were also significantly different in samples collected at the two sites along the Leaf River (p ) 0.02). While only three samples were collected at the first location along the Leaf River, ∑PBDE concentrations ranged from 0.7 to 2.3 ng/g wet weight, whereas the 10 catfish collected at the second location had concentrations ranging from 3.8 to 23.3 ng/g wet weight. Consistent with findings of recent reports (29, 30), the correlation observed between wet weight PBDE levels in all fish and lipid content was very low (r ) -0.39, p < 0.01). BDEs 47, 99, 100, 153, and 154 were detected in all samples and were consistently the dominant contributors to the total
TABLE 1. Wet Weight and Lipid Adjusted Total PBDE Concentrations by Fish and Sample Type (A) and in Wild-Caught Catfish by Sample Location (B) (A) In Fish by Sample Type wild-caught fillet (N ) 24)
farm-raised
all fish (N ) 61)
all (N ) 33)
whole (N ) 9)
all (N ) 28)
fillet (N ) 23)
dressed (N ) 2)
nuggets (N ) 3)
mean (SE) median range
3.4 (0.6) 0.9 0.3-23.3
5.8 (0.9) 4.4a 0.4-23.3
Wet Weight (ng/g) 3.9 (0.6) 10.9 (2.1) b 2.7 10.6 0.4-11.4 3.8-23.3
0.5 (0.03) 0.5c 0.3-0.8
0.5 (0.03) 0.5d 0.3-0.8
0.5 (0.04) 0.5 0.47-0.55
0.6 (0.1) 0.6 0.5-0.8
mean (SE) median range
499 (125) 120 3.6-4730
916 (205) 360a 80.8-4730
Lipid Weight (ng/g lipid) 416 (85.4) 2250 (502) 6.5 (0.4) b 227 1670 5.9c 80.8-1720 536-4730 3.6-11.7
6.2 (0.4) 5.8d 3.6-9.5
10.4 (1.3) 10.4 9.1-11.7
6.6 (1.0) 5.8 5.4-8.7
(B) In Wild-Caught Catfish by Sample Location characteristic
all wild-caught fish (N ) 33)
Mississippi River (N ) 6)
mean (SE) median range
5.8 (0.9) 4.4 0.4-23.3
4.1 (0.8) 4.4 2.1-7.0
mean (SE) median range
916 (205) 360 80.8-4730
331 (159) 199 80.8-1110
Pearl River (N ) 5)
Ross Barnett Spillway (N ) 9)
Leaf River 1 (N ) 3)
Leaf River 2 (N ) 10)
Wet Weight (ng/g) 7.8 (1.1) 2.1 (0.4) 7.0 2.1 5.8-11.4 0.4-4.8
1.6 (0.4) 1.7 0.7-2.3
10.4 (1.9) 9.8 3.8-23.3
