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Environmental Monitoring and Assessment

, Volume 185, Issue 12, pp 10351–10364 | Cite as

A national probabilistic study of polybrominated diphenyl ethers in fish from US lakes and reservoirs

  • Leanne L. StahlEmail author
  • Blaine D. Snyder
  • Anthony R. Olsen
  • Lynn S. Walters
Article

Abstract

Polybrominated diphenyl ethers (PBDEs) are persistent, bioaccumulative, and toxic chemicals that are present in air, water, soil, sediment, and biota (including fish). Most previous studies of PBDEs in fish were spatially focused on targeted waterbodies. National estimates were developed for PBDEs in fish from lakes and reservoirs of the conterminous US (excluding the Laurentian Great Lakes) using an unequal probability design. Predator (fillet) and bottom-dweller (whole-body) composites were collected during 2003 from 166 lakes selected randomly from the target population of 147,343 lakes. Both composite types comprised nationally representative samples that were extrapolated to the sampled population of 76,559 and 46,190 lakes for predators and bottom dwellers, respectively. Fish were analyzed for 34 individual PBDE congeners and six co-eluting congener pairs representing a total of 46 PBDEs. All samples contained detectable levels of PBDEs, and BDE-47 predominated. The maximum aggregated sums of congeners ranged from 38.3 ng/g (predators) to 125 ng/g (bottom dwellers). Maximum concentrations in fish from this national probabilistic study exceeded those reported from recent targeted studies of US inland lakes, but were lower than those from Great Lakes studies. The probabilistic design allowed the development of cumulative distribution functions to quantify PBDE concentrations versus the cumulative number of US lakes from the sampled population.

Keywords

Fish tissue Polybrominated diphenyl ethers Lakes Probabilistic survey 

Notes

Acknowledgments

This study was funded by the US Environmental Protection Agency, and technical support was provided under EPA Contracts EP-C-04-030, ET-W-06-046, and EP-C-09-019, MOBIS Contract GS-23F-9820, and Sample Control Center Contract 68-C-98-139. The manuscript has been subjected to review and approved for publication by US EPA’s Office of Research and Development and EPA’s Office of Water. Approval does not signify that the contents reflect the views of the Agency, nor does mention of trade names or commercial products constitute endorsement or recommendation for use.

This study was made possible by the collaborative efforts of US EPA’s Office of Water, EPA’s Office of Research and Development, and a national network of state, tribal, and federal agency partners. Deep appreciation is expressed to all staff in the participating agencies who conducted lake reconnaissance, planned sampling logistics, and collected fish samples. Technical support was also provided by study team members from Tetra Tech, Inc. (Jennifer Flippen, Erik Leppo, Ann Roseberry Lincoln, and Jennifer Linder), and CSC (Harry McCarty and Michael Walsh). Appreciation is also expressed to Elizabeth Murphy (Great Lakes National Program Office) and Chris Schmitt (US Geological Survey) for their technical review of this paper.

References

  1. Ackerman, L. K., Schwindt, A. R., Massey Simonich, S. L., Koch, D. C., Blett, T. F., Schreck, C. B., et al. (2008). Atmospherically deposited PBDEs, pesticides, PCBs, and PAHs in Western U.S. National Park fish: concentrations and consumption guidelines. Environmental Science and Technology, 42(7), 2334–2341.CrossRefGoogle Scholar
  2. Agency for Toxic Substances and Disease Registry (ATSDR). (2004). Toxicological profile for polybrominated biphenyls and polybrominated diphenyl ethers. (pp. 619). Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service. Available from www.atsdr.cdc.gov/toxprofiles/tp68.pdf.
  3. Betts, K. S. (2008). Unwelcome guest: PBDEs in indoor dust. Environmental Health Perspectives, 116(5), A202–208.CrossRefGoogle Scholar
  4. Bruchajzer, E. (2011). Porphyrogenic effect of pentabromodiphenyl ether after repeated administration to rats. Archives of Toxicology, 85(8), 965–974.CrossRefGoogle Scholar
  5. Burreau, S., Broman, D., & Orn, U. (2000). Tissue distribution of 2,2',4,4'-tetrabromo[14C]diphenyl ether ([14C]-PBDE 47) in pike (Esox lucius) after dietary exposure—a time series study using whole body autoradiography. Chemosphere, 40(9–11), 977–985.CrossRefGoogle Scholar
  6. Chen, D., La Guardia, M. J., Luellen, D. R., Harvey, E., Mainor, T. M., & Hale, R. C. (2011). Do temporal and geographical patterns of HBCD and PBDE flame retardants in U.S. fish reflect evolving industrial usage? Environmental Science and Technology, 45(19), 8254–8261.CrossRefGoogle Scholar
  7. Costa, L. G., Giordano, G., Tagliaferri, S., Caglieri, A., & Mutti, A. (2008). Polybrominated diphenyl ether (PBDE) flame retardants: environmental contamination, human body burden and potential adverse health effects. Acta Bio-Medica, 79(3), 172–183.Google Scholar
  8. Daniels, J. L., Pan, I. J., Jones, R., Anderson, S., Patterson, D. G., Jr., Needham, L. L., et al. (2010). Individual characteristics associated with PBDE levels in U.S. human milk samples. Environmental Health Perspectives, 118(1), 155–160.Google Scholar
  9. Darnerud, P. O. (2003). Toxic effects of brominated flame retardants in man and in wildlife. Environment International, 29(6), 841–853.CrossRefGoogle Scholar
  10. de Boer, J., & Cofino, W. P. (2002). First world-wide interlaboratory study on polybrominated diphenylethers (PBDEs). Chemosphere, 46(5), 625–633.CrossRefGoogle Scholar
  11. de Wit, C. A. (2002). An overview of brominated flame retardants in the environment. Chemosphere, 46(5), 583–624.CrossRefGoogle Scholar
  12. Dodder, N. G., Strandberg, B., & Hites, R. A. (2002). Concentrations and spatial variations of polybrominated diphenyl ethers and several organochlorine compounds in fishes from the Northeastern United States. Environmental Science and Technology, 36(2), 146–151.CrossRefGoogle Scholar
  13. Dunnick, J. K., & Nyska, A. (2009). Characterization of liver toxicity in F344/N rats and B6C3F1 mice after exposure to a flame retardant containing lower molecular weight polybrominated diphenyl ethers. Experimental and Toxicologic Pathology, 61(1), 1–12.CrossRefGoogle Scholar
  14. Gouin, T., & Harner, T. (2003). Modeling the environmental fate of the polybrominated diphenyl ethers. Environment International, 29(6), 717–724.CrossRefGoogle Scholar
  15. Guo, Y., Meng, X. Z., Tang, H. L., Mai, B. X., & Zeng, E. Y. (2008). Distribution of polybrominated diphenyl ethers in fish tissues from the Pearl River Delta, China: levels, compositions, and potential sources. Environmental Toxicology and Chemistry, 27(3), 576–582.CrossRefGoogle Scholar
  16. Hale, R. C., Alaee, M., Manchester-Neesvig, J. B., Stapleton, H. M., & Ikonomou, M. G. (2003). Polybrominated diphenyl ether flame retardants in the North American environment. Environment International, 29(6), 771–779.CrossRefGoogle Scholar
  17. Hale, R. C., La Guardia, M. J., Harvey, E. P., Mainor, T. M., Duff, W. H., & Gaylor, M. O. (2001). Polybrominated diphenyl ether flame retardants in Virginia freshwater fishes (USA). Environmental Science and Technology, 35(23), 4585–4591.CrossRefGoogle Scholar
  18. Hale, R. C., La Guardia, M. J., Harvey, E. P., Mainor, T. M., Duff, W. H., Gaylor, M. O., et al. (2000). Comparison of brominated diphenyl ether fire retardant and organochlorine burdens in fish from Virginia rivers (USA). Organohalogen Compounds, 47, 65–68.Google Scholar
  19. Hallgren, S., & Darnerud, P. O. (2002). Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and chlorinated paraffins (CPs) in rats-testing interactions and mechanisms for thyroid hormone effects. Toxicology, 177(2–3), 227–243.CrossRefGoogle Scholar
  20. Hayward, D., Wong, J., & Krynitsky, A. J. (2007). Polybrominated diphenyl ethers and polychlorinated biphenyls in commercially wild caught and farm-raised fish fillets in the United States. Environmental Research, 103(1), 46–54.CrossRefGoogle Scholar
  21. Hites, R. A. (2004). Polybrominated diphenyl ethers in the environment and in people: a meta-analysis of concentrations. Environmental Science and Technology, 38(4), 945–956.CrossRefGoogle Scholar
  22. Hites, R. A., Foran, J. A., Schwager, S. J., Knuth, B. A., Hamilton, M. C., & Carpenter, D. O. (2004). Global assessment of polybrominated diphenyl ethers in farmed and wild salmon. Environmental Science and Technology, 38(19), 4945–4949.CrossRefGoogle Scholar
  23. Integrated Risk Information System (ITIS) (2008). Toxicological Review of 2,2',4,4'-Tetrabromodiphenyl Ether (BDE-47) (CAS No. 5436-43-1). (EPA/635/R-07/005F, pp. 85). Washington, DC: U.S. Environmental Protection Agency, Environmental Criteria and Assessment OfficeGoogle Scholar
  24. Johnson, A., & Olson, N. (2001). Analysis and occurrence of polybrominated diphenyl ethers in Washington State freshwater fish. Archives of Environmental Contamination and Toxicology, 41(3), 339–344.CrossRefGoogle Scholar
  25. Klasing, S. and Brodberg, R. (2011). Development of Fish Contaminant Goals and Advisory Tissue Levels for Common Contaminants in California Sport Fish: Polybrominated Diphenyl Ethers (PBDEs). (pp. 40). Oakland, CA: California Environmental Protection Agency, Office of Environmental Health Hazard Assessment, Pesticide and Environmental Toxicology Branch.Google Scholar
  26. Kuo, Y. M., Sepulveda, M. S., Sutton, T. M., Ochoa-Acuna, H. G., Muir, A. M., Miller, B., et al. (2010). Bioaccumulation and biotransformation of decabromodiphenyl ether and effects on daily growth in juvenile lake whitefish (Coregonus clupeaformis). Ecotoxicology, 19(4), 751–760.CrossRefGoogle Scholar
  27. Kuriyama, S. N., Wanner, A., Fidalgo-Neto, A. A., Talsness, C. E., Koerner, W., & Chahoud, I. (2007). Developmental exposure to low-dose PBDE-99: tissue distribution and thyroid hormone levels. Toxicology, 242(1–3), 80–90.CrossRefGoogle Scholar
  28. La Guardia, M. J., Hale, R. C., & Harvey, E. (2006). Detailed polybrominated diphenyl ether (PBDE) congener composition of the widely used Penta-, Octa-, and Deca-PBDE technical flame-retardant mixtures. Environmental Science and Technology, 40(20), 6247–6254.CrossRefGoogle Scholar
  29. Lorber, M. (2008). Exposure of Americans to polybrominated diphenyl ethers. Journal of Exposure Science & Environmental Epidemiology, 18, 2–19.CrossRefGoogle Scholar
  30. Luross, J. M., Alaee, M., Sergeant, D. B., Whittle, D. M., & Solomon, K. R. (2000). Spatial and temporal distribution of polybrominated diphenyl ethers in Lake Trout from the Great Lakes. Organohalogen Compounds, 47, 73–76.Google Scholar
  31. Manchester-Neesvig, J. B., Valters, K., & Sonzogni, W. C. (2001). Comparison of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) in Lake Michigan salmonids. Environmental Science and Technology, 35(6), 1072–1077.CrossRefGoogle Scholar
  32. Mizukawa, K., Takada, H., Takeuchi, I., Ikemoto, T., Omori, K., & Tsuchiya, K. (2009). Bioconcentration and biomagnification of polybrominated diphenyl ethers (PBDEs) through lower-trophic-level coastal marine food web. Marine Pollution Bulletin, 58(8), 1217–1224.CrossRefGoogle Scholar
  33. Noren, K., & Meironyte, D. (2000). Certain organochlorine and organobromine contaminants in Swedish human milk in perspective of past 20–30 years. Chemosphere, 40(9–11), 1111–1123.CrossRefGoogle Scholar
  34. Olsen, A. R., Snyder, B. D., Stahl, L. L., & Pitt, J. L. (2009). Survey design for lakes and reservoirs in the United States to assess contaminants in fish tissue. Environmental Monitoring and Assessment, 150(1–4), 91–100.CrossRefGoogle Scholar
  35. Perez-Fuentetaja, A., Lupton, S., Clapsadl, M., Samara, F., Gatto, L., Biniakewitz, R., et al. (2010). PCB and PBDE levels in wild common carp (Cyprinus carpio) from eastern Lake Erie. Chemosphere, 81(4), 541–547.CrossRefGoogle Scholar
  36. Development Core Team, R. (2007). The R project for statistical computing. Vienna: R Development Core Team.Google Scholar
  37. Rahman, F., Langford, K. H., Scrimshaw, M. D., & Lester, J. N. (2001). Polybrominated diphenyl ether (PBDE) flame retardants. Science of the Total Environment, 275(1–3), 1–17.CrossRefGoogle Scholar
  38. Rayne, S., Ikonomou, M. G., & Antcliffe, B. (2003). Rapidly increasing polybrominated diphenyl ether concentrations in the Columbia River system from 1992 to 2000. Environmental Science and Technology, 37(13), 2847–2854.CrossRefGoogle Scholar
  39. Rice, C. P., Chernyak, S. M., Begnoche, L., Quintal, R., & Hickey, J. (2002). Comparisons of PBDE composition and concentration in fish collected from the Detroit River, MI and Des Plaines River, IL. Chemosphere, 49(7), 731–737.CrossRefGoogle Scholar
  40. Schecter, A., Colacino, J., Patel, K., Kannan, K., Yun, S. H., Haffner, D., et al. (2010). Polybrominated diphenyl ether levels in foodstuffs collected from three locations from the United States. Toxicology and Applied Pharmacology, 243(2), 217–224.CrossRefGoogle Scholar
  41. Schecter, A., Harris, T. R., Shah, N., Musumba, A., & Papke, O. (2008). Brominated flame retardants in US food. Molecular Nutrition & Food Research, 52(2), 266–272.CrossRefGoogle Scholar
  42. Schecter, A., Papke, O., Harris, T. R., Tung, K. C., Musumba, A., Olson, J., et al. (2006). Polybrominated diphenyl ether (PBDE) levels in an expanded market basket survey of U.S. food and estimated PBDE dietary intake by age and sex. Environmental Health Perspectives, 114(10), 1515–1520.CrossRefGoogle Scholar
  43. Schecter, A., Papke, O., Tung, K. C., Staskal, D., & Birnbaum, L. (2004). Polybrominated diphenyl ethers contamination of United States food. Environmental Science and Technology, 38(20), 5306–5311.CrossRefGoogle Scholar
  44. Schecter, A., Pavuk, M., Papke, O., Ryan, J. J., Birnbaum, L., & Rosen, R. (2003). Polybrominated diphenyl ethers (PBDEs) in U.S. mothers’ milk. Environmental Health Perspectives, 111(14), 1723–1729.CrossRefGoogle Scholar
  45. Shaw, S. D., Berger, M. L., Brenner, D., Carpenter, D. O., Tao, L., Hong, C. S., et al. (2008). Polybrominated diphenyl ethers (PBDEs) in farmed and wild salmon marketed in the Northeastern United States. Chemosphere, 71(8), 1422–1431.CrossRefGoogle Scholar
  46. Sinkkonen, S., Rantalainen, A. L., Paasivirta, J., & Lahtipera, M. (2004). Polybrominated methoxy diphenyl ethers (MeO-PBDEs) in fish and guillemot of Baltic, Atlantic and Arctic environments. Chemosphere, 56(8), 767–775.CrossRefGoogle Scholar
  47. Sloan, C. A., Anulacion, B. F., Bolton, J. L., Boyd, D., Olson, O. P., Sol, S. Y., et al. (2010). Polybrominated diphenyl ethers in outmigrant juvenile Chinook salmon from the lower Columbia River and Estuary and Puget Sound, Washington. Archives of Environmental Contamination and Toxicology, 58(2), 403–414.CrossRefGoogle Scholar
  48. Stahl, L. L., Snyder, B. D., Olsen, A. R., & Pitt, J. L. (2009). Contaminants in fish tissue from US lakes and reservoirs: a national probabilistic study. Environmental Monitoring and Assessment, 150(1–4), 3–19.CrossRefGoogle Scholar
  49. Stapleton, H. M., Alaee, M., Letcher, R. J., & Baker, J. E. (2004). Debromination of the flame retardant decabromodiphenyl ether by juvenile carp (Cyprinus carpio) following dietary exposure. Environmental Science and Technology, 38(1), 112–119.CrossRefGoogle Scholar
  50. Staskal, D. F., Scott, L. L., Haws, L. C., Luksemburg, W. J., Birnbaum, L. S., Urban, J. D., et al. (2008). Assessment of polybrominated diphenyl ether exposures and health risks associated with consumption of southern Mississippi catfish. Environmental Science and Technology, 42(17), 6755–6761.CrossRefGoogle Scholar
  51. Stevens, D. L., & Olsen, A. R. (2004). Spatially balanced sampling of natural resources. Journal of the American Statistical Association, 99(465), 262–278.CrossRefGoogle Scholar
  52. Streets, S. S., Henderson, S. A., Stoner, A. D., Carlson, D. L., Simcik, M. F., & Swackhamer, D. L. (2006). Partitioning and bioaccumulation of PBDEs and PCBs in Lake Michigan. Environmental Science and Technology, 40(23), 7263–7269.CrossRefGoogle Scholar
  53. Turyk, M. E., Persky, V. W., Imm, P., Knobeloch, L., Chatterton, R., & Anderson, H. A. (2008). Hormone disruption by PBDEs in adult male sport fish consumers. Environmental Health Perspectives, 116(12), 1635–1641.CrossRefGoogle Scholar
  54. U.S. Environmental Protection Agency (USEPA) (2000a). Guidance for assessing chemical contaminant data for use in fish advisories. (Vol. 1: Fish Sampling and Analysis, EPA-823-B-00-007, pp. 485). Washington, DC: U.S. Environmental Protection Agency, Office of Water, Office of Science and TechnologyGoogle Scholar
  55. U.S. Environmental Protection Agency (USEPA) (2000b). Field sampling plan for the national study of chemical residues in lake fish tissue. (EPA-823-R-02-004, pp. 40). Washington, DC: U.S. Environmental Protection Agency, Office of Water, Office of Science and Technology.Google Scholar
  56. U.S. Environmental Protection Agency (USEPA) (2003). Brominated diphenyl ethers in water soil, sediment and tissue by HRGC/HRMS [Draft]. (EPA-821-R-07-005, pp. 87). Washington, DC: U.S. Environmental Protection Agency, Office of Water, Office of Science and Technology.Google Scholar
  57. U.S. Environmental Protection Agency (USEPA) (2005). Quality assurance report for the national study of chemical residues in lake fish tissue: analytical data for years 1 through 4. (EPA-823-R-05-005, pp. 57). Washington, DC: U.S. Environmental Protection Agency, Office of Water, Office of Science and Technology.Google Scholar
  58. U.S. Environmental Protection Agency (USEPA) (2009). The national study of chemical residues in lake fish tissue. (EPA-823-R-09-006, pp. 242). Washington, DC: U.S. Environmental Protection Agency, Office of Water, Office of Science and Technology.Google Scholar
  59. U.S. Environmental Protection Agency (USEPA) (2010a). An exposure assessment of polybrominated diphenyl ethers (PBDE). (EPA/600/R-08/086F, pp. 387). Washington, DC: U.S. Environmental Protection AgencyGoogle Scholar
  60. U.S. Environmental Protection Agency (USEPA) (2010b). DecaBDE phase-out initiative. Washington, DC: U.S. Environmental Protection Agency, Office of Pollution Prevention and Toxics.Google Scholar
  61. Valters, K., Li, H., Alaee, M., D’Sa, I., Marsh, G., Bergman, A., et al. (2005). Polybrominated diphenyl ethers and hydroxylated and methoxylated brominated and chlorinated analogues in the plasma of fish from the Detroit River. Environmental Science and Technology, 39(15), 5612–5619.CrossRefGoogle Scholar
  62. Vonderheide, A. P., Mueller, K. E., Meija, J., & Welsh, G. L. (2008). Polybrominated diphenyl ethers: causes for concern and knowledge gaps regarding environmental distribution, fate and toxicity. Science of the Total Environment, 400(1–3), 425–436.CrossRefGoogle Scholar
  63. Wolkers, H., Van Bavel, B., Derocher, A. E., Wiig, O., Kovacs, K. M., Lydersen, C., et al. (2004). Congener-specific accumulation and food chain transfer of polybrominated diphenyl ethers in two Arctic food chains. Environmental Science and Technology, 38(6), 1667–1674.CrossRefGoogle Scholar
  64. Xia, K., Luo, M. B., Lusk, C., Armbrust, K., Skinner, L., & Sloan, R. (2008). Polybrominated diphenyl ethers (PBDEs) in biota representing different trophic levels of the Hudson River, New York: from 1999 to 2005. Environmental Science and Technology, 42(12), 4331–4337.CrossRefGoogle Scholar
  65. Zar, J. H. (1999). Biostatistical analysis (4th ed.). Upper Saddle River: Prentice Hall.Google Scholar
  66. Zhu, L. Y., & Hites, R. A. (2004). Temporal trends and spatial distributions of brominated flame retardants in archived fishes from the Great Lakes. Environmental Science and Technology, 38(10), 2779–2784.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2013

Authors and Affiliations

  • Leanne L. Stahl
    • 1
    Email author
  • Blaine D. Snyder
    • 2
  • Anthony R. Olsen
    • 3
  • Lynn S. Walters
    • 4
  1. 1.OW/Office of Science and TechnologyU.S. Environmental Protection AgencyWashingtonUSA
  2. 2.Center for Ecological SciencesTetra Tech, Inc.Owings MillsUSA
  3. 3.ORD/National Health and Environmental Effects Laboratory, Western Ecology DivisionU.S. Environmental Protection AgencyCorvallisUSA
  4. 4.CSCAlexandriaUSA

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