POLYBROMINATED DIPHENYL ETHERS (PBDES) IN FARMED SALMON (Salmo salar) FROM MAINE AND EASTERN CANADA
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1 Organohalogen Compounds, Vol. 67: , 2005 Copyright 2005 Dioxin 2005, ISBN POLYBROMINATED DIPHENYL ETHERS (PBDES) IN FARMED SALMON (Salmo salar) FROM MAINE AND EASTERN CANADA Susan D. Shaw 1, Anna Bourakovsky 1a, Diane Brenner 1, David O. Carpenter 2, Lin Tao 3, Kurunthachalam Kannan 3, and Chia-Swee Hong 3 1 Marine Environmental Research Institute, PO Box 1652, Blue Hill, ME USA 2 Institute for Health and the Environment, University at Albany, Rensselaer, NY USA 3 Wadsworth Center, New York State Department of Health, Albany, NY USA Introduction Brominated flame retardants, especially the polybrominated diphenyl ethers (PBDEs), are ubiquitous persistent organic pollutants (POPs) that biomagnify and are associated with endocrine-disrupting and neurodevelopmental effects 1 in rodent studies. Concern has increased about human health risks in tandem with evidence of rising PBDE concentrations in human breast milk 2, particularly in the United States, where PBDE levels in human milk are an order of magnitude higher than those in other countries 3,4. While PBDEs are still in extensive production and use, the relationship between human levels and dietary intake is not well characterized, and data on PBDE levels consumed in the US are quite limited. A recent survey found that PBDE levels in US foods are higher than levels in food from other countries, and the highest PBDE levels are in fish such as salmon as compared with other farm-raised animals (chicken, beef, pork) destined for human consumption 5. Over the past decade, the farmed salmon industry has rapidly expanded in the US, especially in Maine where production tripled between 1990 and It is estimated that Maine supplies ~ 18% of US domestic consumption of farmed salmon, and virtually 100% is sold to consumers in the New England region. Along with Maine, Canada and Chile are the main sources of farmed salmon sold in this region. Since 1987, per capita consumption of salmon has grown by more than 26% annually; by 2000, more than half of the salmon consumed was farmed 7. Currently, an estimated 23.1 million US residents eat salmon more often than once a month, 1.3 million eat salmon at least once a week, and 180,000 eat salmon more often than twice a week 8. Because the levels of POPs can be significantly higher in farm-raised salmon than in wild salmon 9,10, the possible contribution of PBDEs to human body burdens resulting from farmed salmon consumption could clearly be of concern for heavy consumers. Here we provide results on PBDE concentrations in farmed and wild salmon marketed to consumers in the northeast region, including farmed Atlantic salmon (Salmo salar) produced in Maine and eastern Canada, wild Alaskan Chinook salmon (Oncorhynchus tshawytscha),and organically farmed salmon from Norway labeled as natural farmed salmon. Methods and Materials Samples. A total of 70 farmed and wild salmon were collected from wholesale and retail outlets in Maine between August 2003 and May The farmed salmon represented six farming locations in three regions, including two farms in eastern Maine, three in eastern Canada, and one in Norway. Wild Chinook salmon from Alaska were also purchased from a wholesale supplier in Maine. Suppliers provided information on the origin (region and farm) of the fish. Ten whole fish were obtained from each farm, nine of which were randomly pooled into three composite samples of three fish each. We analyzed both skin-on and skin-off samples to determine whether the presence of skin contributes to contaminant loads. The whole fish were thawed, weighed, measured, filleted and deboned to yield two fillets per fish, one with skin on and one with skin removed. The fillets from three fish were then homogenized in a high speed processor to make two composites (skin-on/off), resulting in a total of 42 composite samples for analysis. Samples were subdivided into smaller replicate portions of 100g, and frozen at -20 C. in Please send requests for reprints to Dr. Susan D. Shaw, Marine Environmental Research Institute, Center for Marine Studies, PO Box 1652, 55 Main Street, Blue Hill ME 04614, USA, Phone: , FAX: , sshaw@meriresearch.org
2 SHAW ET AL. Organohalogen Compounds, Vol. 67, borosilicate glass containers with PTFE-lined lids. The samples were sent packed on ice or frozen gelpacks to the Wadsworth Center, NY State Department of Health, Albany, NY, where they were stored at - 20 C. prior to analysis. Chemical Analysis. All salmon samples were analyzed for nine PBDE congeners (IUPAC nos. 28, 47, 66, 85, 99, 100, 138, 153, and 154) following the isotope dilution quantification method previously developed 11. Fifteen to twenty grams of wet weight tissue were taken from each composite sample and homogenized with granular sodium sulfate and Soxhlet extracted using a 400 ml 3:1 dichloromethane:hexane mixture for six hours. The extract was concentrated to 11 ml and lipid content was determined gravimetrically using 1 ml of the extract. Known amounts of 13 C-labeled PBDE congeners were added as internal standards to the remaining extract. The extract was cleaned up by gel permeation chromatography (GPC) and then on a multilayer silica gel column and injected into a GC (Hewlett-Packard 6890) coupled with a mass selective detector (Hewlett-Packed, series 5973). Chromatographic separation of PBDE congeners was achieved on a DB-5 capillary high temperature column coated at 0.25 μm (60 m x 0.25 mm i.d.), with column temperature programmed from 100 C (1 min) to 160 C. (3 min) at a rate of 10 C/min, and then to 260 C. at 2 C/min, with a final hold time of 5 min. PBDE congeners were monitored by selected ion monitoring (SIM) at the two most intensive ions at the molecular ion cluster. Method limits of detection limit for individual PBDE congeners ranged from 1 to 10 pg/g, wet weight, depending on the sample matrix and congener. All analyses were conducted in accordance with Wadsworth Center s Quality Assurance and Quality Control protocols. Results and Discussion The total PBDE concentrations found in farmed and wild salmon in this study are relatively low ( 1 ppb, wet weight) but of a similar order of magnitude as those reported in recent studies 10,12,13. Mean levels in all samples from farmed fish (0.92 ng/g, wet weight) exceeded levels found in wild salmon (0.71 ng/g, wet weight), although the difference was not statistically significant. The average concentration of the nine PBDE congeners across all farmed salmon samples from Maine and eastern Canada was 0.89 ng/g, wet weight (7.3 ng/g, lipid), although levels varied by producer within these regions (Fig. 1). The lowest and highest levels (0.5 and 1.1 ng/g, wet weight, respectively) were found in samples from two Canadian farms that used commercial feed from the same source. The farmed bioculture samples from Norway had the second highest PBDE levels found in this study (1.04 ng/g, wet weight). Differences between farmed and wild salmon and those among producers were not significant. PBDE congener profiles in farmed and wild salmon samples were similar, except that the Norwegian samples had higher concentrations of BDE 100 (p=0.035) than farmed salmon from Maine and eastern Canada. As expected, BDE 47 dominated the congener profiles, contributing 38-58% of total measured PBDEs, followed by BDE 99 and BDE 100, accounting for another 21-26% of the total. This pattern is similar to that found in previous studies of fish as well as in most environmental samples and in humans 5. The Norwegian bioculture salmon showed a variation in pattern with BDE 100 contributing more of the total than BDE 99. Total PBDE concentrations reported by Hites and co-workers 10 in farmed salmon from Maine and eastern Canada and those found in salmon fillets analyzed in a US market basket study 4 were slightly higher (~2-3 ppb, wet weight) than levels in our farm-raised salmon samples from this region. However, our study measured fewer congeners, thus the sum of the congener concentrations may be an underestimate of the total PBDE concentration. On a global scale, the results of this study are four- to five-fold lower, respectively, than PBDE concentrations recently reported in farmed salmon from British Columbia 10 and northwestern Europe 12,13, and comparable to levels reported in farmed salmon from Chile 10. Total PBDE concentrations found in
3 SHAW ET AL. Organohalogen Compounds, Vol. 67, our wild salmon samples (0.71 ± 0.46 ng/g, wet weight) were similar to those recently reported in wild Alaskan Chinook (0.5 ng/g, wet weight), but four-fold lower than levels found in wild Chinook from British Columbia 10 and in UK wild salmon 13. Wild salmon from polluted waters such as the Baltic and Lake Michigan contain much higher concentrations of PBDEs 14-16, several orders of magnitude higher than the concentrations reported in this study, but with a similar congener distribution. Although we expected PBDE concentrations and lipid content (%) to be significantly higher in the samples with skin-on, this was not the case. Lipid content in the skin-on samples was only slightly higher than in the samples with skin removed, and in contrast with the pattern for PCBs and chlorinated pesticides, PBDE levels were actually higher in skin-off samples from one Maine farm and two Canadian farms (Fig.2). Also in contrast with other POPs, there was no apparent correlation between the sum PBDE concentrations and the amount of lipid in these samples, which is consistent with results of previous studies of salmon and other seafood species 12. Because most salmon is marketed to consumers with skin on, we used the skin-on samples (n=21) in the analysis. Lipid content of the samples was significantly different between producers [F=23.7, p<.001, df =6,14]. Lipids were highest in the Norwegian bioculture samples (18.4%) and samples from one Maine farm (18.2%), while wild Alaskan samples had the lowest lipid content (7.6%), reflecting differences in diet between wild and farmed fish. Diets high in marine fish oils (30-36%) are favored by the aquaculture industry as an additive that promotes fast growth of fish while raising levels of beneficial omega-3 fatty acids. However, it is likely that these oils contribute substantially to the contamination of farmed salmon by lipophilic POPs. Bioculture salmon diets are generally lower in fish oil content (maximum 28% of the total diet), and claim to be virtually contaminant-free based on monitoring results for ICES7 PCBs. Interestingly, in this study the Norwegian bioculture samples were the highest in fat content, and the PBDE contaminant loading was similar to that of the farmed salmon produced in the region, demonstrating the need to measure PBDEs as well as other halogenated compounds not only in feed but in fish marketed for human consumption. This study shows that farmed salmon produced in the northeast region is contaminated with PBDEs, although concentrations were relatively low compared those found in other studies and similar to those of bioculture salmon from Norway. In view of the elevated body burdens in tissues of US residents and the increasing availability of farmed salmon to the consumer, the ongoing quantification of these compounds in farmed fish is important for human dietary exposure assessment. Acknowledgments This research was supported by the Grayce B. Kerr Fund and the Sasco Foundation. The authors wish to thank Kirk Trabant, Marine Environmental Research Institute, for collection and processing of the salmon samples. References 1. Birnbaum, L. B., Staskal, D. F. (2003). Environ. Health Perspect.112: Meironyté, D., Norén, K, Bergman, A. (1999). J. Toxicol.Environ.Health 58: Schecter, A. J., Pavuk, M., Päpke, O., Ryan, J. J., Birnbaum, L., Rosen, R. (2003). Environ. Health Perspect.111: Environmental Working Group (2004) Schecter, A., Päpke, O., Tung, K-C., Staskal, D., Birnbaum, L. (2004). Environ.Sci.Tech. 38: Gardner Pinfold (2003). Report to the ME Department of Marine Resources. Gardner Pinfold Consulting Economists, Ltd., 84 pp. 7. Fisheries Global Information System (FI-GIS), United Nations Food and Agriculture
4 SHAW ET AL. Organohalogen Compounds, Vol. 67, Organization (2004). Available at: 8. Redmayne, P. (2000). SeaFood Business. August Hites, R. A., Foran, J. A., Carpenter, D.O., Hamilton, M. C., Knuth, B. A., Schwager, S. J. (2004). Science 303: Hites, R. A., Foran, J. A., Schwager, S. J., Knuth, B. A., Hamilton, M. C., Carpenter, D.O. (2004). Environ.Sci.Tech. 38(19): Loganathan B.G., Kannan K, Watanabe I, Kawano M., Irvine K., Kumar S., Sikka H.C. (1995). Environ.Sci.Tech. 29 (7): Bethune, C., Nielsen, J., Julshamn, K. (2004). Organohalogen Compounds 66: Jacobs, M., Covaci A., Schepens, P. (2002). Environ. Sci. Tech. 36: Bergman, A. (2000). Organohalogen Compounds 47: Darnerud, P.O., Eriksen, G. S., Jóhannesson, T., Larsen, P. B., Viluksela, M. (2001). Environ. Health Perspect 109 (Suppl. 1): Manchester-Neesvig, J., Valters, K., Sonzogni, W.(2001). Environ. Sci. Tech. 35:
5 SHAW ET AL. Organohalogen Compounds, Vol. 67, ng/g, ww NOR ME1 ME2 CAN1 CAN2 CAN3 AK Fig. 1. PBDE concentrations (ng/g, wet weight) in salmon by producer ng/g, ww Skin off Skin on AK CAN3 CAN2 CAN1 ME2 ME1 NOR Fig. 2. PBDE concentrations (ng/g, ww) in skin-on and skin-off samples by producer
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