Effectiveness of Various Exposure Metrics in Defining Dose-Response Relationships for Mink (Mustela vison) Exposed to Polychlorinated Biphenyls

Article

Abstract

We conducted a quantitative analysis of published results from more than 50 tests of polychlorinated biphenyl (PCB) effects on mink reproduction, which provided a basis for evaluating how well different methods of measuring and assessing PCB concentrations can approximate a toxicologically relevant dose for this endpoint. Several dose metrics were identified for comparison. Dietary dose metrics included the daily intake of total PCBs and the daily intake of 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity equivalence concentrations (TECs), calculated using World Health Organization toxicity equivalence factors (TEFs). Internal dose metrics included whole-body total PCBs, whole-body TECs calculated using World Health Organization TEFs, and whole-body TECs calculated using alternative TEFs specifically identified for internal dose assessment. Accounting for the bioaccumulative potential (i.e., internal dose) of ingested PCBs proved to be more important than accounting for the concentrations of dioxin-like PCB congeners in explaining the observed variation in reproductive success. This was true regardless of whether internal doses were estimated from dietary data based on homolog concentrations (whole-body total PCBs) or congener concentrations (whole-body TECs). For each of the PCB dose metrics, a range of toxicity reference values is identified based on the species-specific PCB toxicity database compiled for this evaluation.

References

  1. Aulerich RJ, Ringer RK (1977) Current status of PCB toxicity to mink, and effect on their reproduction. Arch Environ Contam Toxicol 6:279–292CrossRefGoogle Scholar
  2. Aulerich RJ, Bursian SJ, Breslin WJ, Olson BA, Ringer RK (1985) Toxicological manifestations of 2,4,5-, 2′, 4′, 5′-, 2,3,6,2′, 3′, 6′-, and 3,4,5,3′, 4′, 5′- hexachlorobiphenyl and Aroclor 1254 in mink. J Toxicol Environ Health 15:63–79CrossRefGoogle Scholar
  3. Beckett KJ, Millsap SD, Blankenship AL, Zwiernik MJ, Giesy JP, Bursian SJ (2005) Squamous epithelial lesion of the mandibles and maxillae of wild mink (Mustela vison) naturally exposed to polychlorinated biphenyls. Environ Toxicol Chem 24:674–677CrossRefGoogle Scholar
  4. Bleavins MR, Aulerich RJ, Ringer RK (1980) Polychlorinated biphenyls (Aroclors 1016 and 1242): Effects on survival and reproduction in mink and ferrets. Arch Environ Contam Toxicol 9:627–635CrossRefGoogle Scholar
  5. Brunström B, Lund B, Bergman Å, Asplund L, Athanassiadis I, Athanasiadou M, Jensen S, Örberg J (2001) Reproductive toxicity in mink (Mustela vison) chronically exposed to environmentally relevant polychlorinated biphenyl concentrations. Environ Toxicol Chem 20:2318–2327CrossRefGoogle Scholar
  6. Burgin DE, Diliberto JJ, Derr-Yellin EC, Kannan N, Kodavanti PRS, Birnbaum LS (2001) Differential effects of two lots of Aroclor 1254 on enzyme induction, thyroid hormones, and oxidative stress. Environ Health Perspect 109:1163–1168CrossRefGoogle Scholar
  7. Bursian SJ, Aulerich RJ, Yamini B, Tillitt DE (2003) Dietary exposure of mink to fish from the Housatonic River: Effects on reproduction and survival. Submitted to Weston Solutions, Inc., West Chester, PA. Available at http://www.epa.gov/region1/ge/thesite/restofriver/reports/final_era/SupportingInformation and Studies for the HousatonicRiverProject/Dietary Exposure of Mink.pdf)
  8. Bursian SJ, Beckett KJ, Yamini B, Martin PA, Kannan K, Shields KL, Mohr FC (2006a) Assessment of effects in mink caused by consumption of carp collected from the Saginaw River, Michigan, USA. Arch Environ Contam Toxicol 50:614–623CrossRefGoogle Scholar
  9. Bursian SJ, Sharma C, Aulerich RJ, Yamini B, Mitchell RR, Orazio CE, Moore DRJ, Svirsky S, Tillitt DE (2006b) Dietary exposure of mink (Mustela vison) to fish from the Housatonic River, Berkshire County, Massachusetts, USA: Effects on reproduction, kit growth, and survival. Environ Toxicol Chem 25:1533–1540CrossRefGoogle Scholar
  10. Compton R, Sigal EA (1999) The use of toxicity equivalency factors (TEFs) in ecological risk assessment: Strengths and limitations. Human Ecol Risk Assess 5:33–42Google Scholar
  11. De Voogt P, Brinkman UATh (1989) Production, properties and usage of polychlorinated biphenyls. In: Kimbrough RD, Jensen AA (eds) Halogenated Biphenyls, Terphenyls, Naphthalenes, Dibenzodioxins and Related Products, 2nd ed. Elsevier, Amsterdam, pp 1–45Google Scholar
  12. Den Boer MH (1984) Reproduction decline of harbor seals: PCBs in the food and their effect on mink. Annual report. Rijksinstituut voor Natuurbeheer, Leersum, The Netherlands, pp 77–86Google Scholar
  13. DeVito MJ, Diliberto JJ, Ross DG, Menache MG, Birnbaum LS (1997) Dose-response relationships for polyhalogenated dioxins and dibenzofurans following subchronic treatment in mice. 1. CYP1A1 and CYP1A2 enzyme activity in liver, lung, and skin. Toxicol Appl Pharmacol 147:267–280CrossRefGoogle Scholar
  14. DeVito MJ, Menache MG, Diliberto JJ, Ross DG, Birnbaum LS (2000) Dose-response relationships for induction of CYP1A1 and CYP1A2 enzyme activity in liver, lung, and skin in female mice following subchronic exposure to polychlorinated biphenyls. Toxicol Appl Pharmacol 167:157–172CrossRefGoogle Scholar
  15. Fries GF, Marrow GS (1975) Retention and excretion of 2,3,7,8-tetrachlorodibenzo-p-dioxin by rats. J Agr Food Chem 23:265–269CrossRefGoogle Scholar
  16. Geyer HJ, Werner Schramm K, Feicht EA, Behechti A, Steinberg C, Bruggemann R, Poiger H, Henkelmann B, Kettrup A (2002) Half-lives of tetra-, penta-, hexa-, hepta-, and octachlorodibenzo-p-dioxin in rats, monkeys, and humans – A critical review. Chemosphere 48:631–644CrossRefGoogle Scholar
  17. Giesy JP, Kannan K (1998) Dioxin-like and non-dioxin-like toxic effects of polychlorinated biphenyls (PCBs): Implications for risk assessment. Crit Rev Toxicol 28:511–569CrossRefGoogle Scholar
  18. Halbrook RS, Aulerich RJ, Bursian SJ, Lewis L (1999) Ecological risk assessment in a large river-reservoir: 8. Experimental study of the effects of polychlorinated biphenyls on reproductive success in mink. Environ Toxicol Chem 18:649–654CrossRefGoogle Scholar
  19. Heaton SN, Bursian SJ, Giesy JP, Tillitt DE, Render JA, Jones PD, Verbrugge DA, Kubiak TJ, Aulerich RJ (1995) Dietary exposure of mink to carp from Saginaw Bay, Michigan 1. Effects on reproduction and survival, and the potential risks to wild mink populations. Arch Environ Contam Toxicol 28:334–343CrossRefGoogle Scholar
  20. Hochstein JR, Aulerich RJ, Bursian SJ (1988) Acute toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to mink. Arch Environ Contam Toxicol 17:33–37CrossRefGoogle Scholar
  21. Hornshaw TC, Aulerich RJ, Johnson HE (1983) Feeding Great Lakes fish to mink: Effects on mink and accumulation and elimination of PCBs by mink. J Toxicol Environ Health 11:933–946Google Scholar
  22. Jensen S, Kihlström JE, Olsson M, Lundberg C, Örberg J (1977) Effects of PCB and DDT on mink (Mustela vision) during the reproductive season. Ambio 6:239Google Scholar
  23. Käkelä A, Käkelä R, Hyvärinen H, Asikainen J (2002) Vitamins A1 and A2 in hepatic tissue and subcellular fractions in mink feeding on fish-based diets and exposed to Aroclor 1242. Environ Toxicol Chem 21:397–403CrossRefGoogle Scholar
  24. Kannan N, Hong SH, Oh JR (2005) Non-o,o′-chlorine substituted congeners in commercial polychlorinated biphenyl (PCB) mixtures of the world. Bull Environ Contam Toxicol 75:897–902CrossRefGoogle Scholar
  25. Kihlström JE, Olsson M, Jensen S, Johansson Å, Ahlbom J, Bergman Å (1992) Effects of PCB and different fractions of PCB on the reproduction of the mink (Mustela vison). Ambio 21:563–569Google Scholar
  26. Leonards PEG, de Vries TH, Minnard W, Stuijfzand S, de Voogt P, Cofino WP, van Straalen NM, van Hattum B (1995) Assessment of experimental data on PCB-induced reproduction inhibition in mink, based on an isomer- and congener-specific approach using 2,3,7,8-tetrachlorodibenzo-p-dioxin toxic equivalency. Environ Toxicol Chem 14:639–652CrossRefGoogle Scholar
  27. Leonards PEG, Broekhuizen S, de Voogt P, Van Straalen NM, Brinkman UATh, Cofino WP, van Hattum B (1998) Studies of bioaccumulation and biotransformation of PCBs in mustelids based on concentration and congener patterns in predators and preys. Arch Environ Contam Toxicol 35:654–665CrossRefGoogle Scholar
  28. Ludwig JP, Kurita-Matsuba H, Auman HJ, Ludwig ME, Summer CL, Giesy JP, Tillitt DE, Jones PD (1996) Deformities, PCBs, and TCDD-equivalents in double-crested cormorants (Phalacrocorax auritus) and Caspian terns (Hydroprogne caspia) of the upper Great Lakes 1986-1991: Testing a cause-effect hypothesis. J Great Lakes Res 22:172–197CrossRefGoogle Scholar
  29. Millsap SD, Blankenship AL, Bradley PW, Jones PD, Kay D, Neigh A, Park C, Strause KD, Zwiernik MJ, Giesy JP (2004) Comparison of risk assessment methodologies for exposure of mink to PCBs on the Kalamazoo River, Michigan. Environ Sci Technol 38:6451–6459CrossRefGoogle Scholar
  30. Motulsky HJ, Ransnas LA (1987) Fitting curves to data using nonlinear regression: A practical and nonmathematical review. FASEB J 1:365–374Google Scholar
  31. Murray FJ, Smith FA, Nitschke KD, Huniston CG, Kociba RJ, Schwetz BA (1979) Three-generation reproduction study of rats given 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in the diet. Toxicol Appl Pharmacol 50:241–252CrossRefGoogle Scholar
  32. Pitts GC, Bullard TR (1968) Some interspecific aspects of body composition in mammals. In: Body Composition in Animals and Man. National Academy of Science, Washington, DC, Publ. No. 1598, pp 45–70Google Scholar
  33. Platonow NS, Karstand LH (1973) Dietary effects of polychlorinated biphenyls on mink. Can J Comp Med 37:391–400Google Scholar
  34. Restum JC, Bursian SJ, Giesy JP, Render JA, Helferich WG, Shipp EB, Verbrugge DA, Aulerich RJ (1998) Multigenerational study of the effects of consumption of PCB-contaminated carp from Saginaw Bay, Lake Huron, on mink. 1. Effects on mink reproduction, kit growth and survival, and selected biological parameters. J Toxicol Environ Health A 54:343–375CrossRefGoogle Scholar
  35. Rushneck DR, Beliveau A, Fowler B, Hamilton C, Hoover D, Kaye K, Berg M, Smith T, Telliard WA, Roman H, Ruder E, Ryan L (2004) Concentrations of dioxin-like PCB congeners in unweathered Aroclors by HRGC/HRMS using EPA Method 1668A. Chemosphere 54:79–87CrossRefGoogle Scholar
  36. Safe SH (1997/1998) Limitations of the toxic equivalency factor approach for risk assessment of TCDD and related compounds. Teratogenesis Carcinog Mutagen 17:285–304Google Scholar
  37. Sanderson JT, van den Berg M (1999) Toxic equivalency factors (TEFs) and their use in ecological risk assessment: A successful method when used appropriately. Human Ecol Risk Assess 5:43–52Google Scholar
  38. Stahl BU, Kettrup A, Rozman K (1992) Comparative toxicity of four chlorinated dibenzo-p-dioxins (CDDs) and their mixture. Part I: Acute toxicity and toxic equivalency factors (TEFs). Arch Toxicol 66:471–477CrossRefGoogle Scholar
  39. Takasuga T, Senthilkumar K, Matsumura T, Shiozaki K, Sakai S (2006) Isotope dilution analysis of polychlorinated biphenyls (PCBs) in transformer oil and global commercial PCB formulations by high resolution gas chromatography-high resolution mass spectrometry. Chemosphere 62:469–484CrossRefGoogle Scholar
  40. Taniyasu S, Falandysz J, Świętojanśka A, Flisak M, Horii Y, Hanari N, Yamashita N (2005) Clophen A60 composition and content of CBs, CNs, CDFs, and CDDs after 2D-HPLC, HRGC/LRMS, and HRGC/HRMS separation and quantification. J Environ Sci Health A 40:43–61CrossRefGoogle Scholar
  41. Tillitt DE, Gale RW, Meadows JC, Zajicek JL, Peterman PH, Heaton SN, Jones PD, Bursian SJ Kubiak TJ, Giesy JO, Aulerich RJ (1996) Dietary exposure of mink to carp from Saginaw Bay. 3. Characterization of dietary exposure to planar halogenated hydrocarbons, dioxin equivalents, and biomagnification. Environ Sci Technol 30:283–291CrossRefGoogle Scholar
  42. USEPA (U.S. Environmental Protection Agency) (1995) Great Lakes Water Quality Initiative criteria documents for the protection of wildlife: DDT, mercury, 2,3,7,8-TCDD, PCBs, EPA-820-B-95-008, U.S. EPA, Washington, DCGoogle Scholar
  43. USEPA (U.S. Environmental Protection Agency) (2003) Framework for application of the toxicity equivalence methodology for polychlorinated dioxins, furans and biphenyls in ecological risk assessment, preliminary draft. U.S. EPA, Washington, DCGoogle Scholar
  44. Van den Berg M, De Jongh J, Poiger H, Olson JR (1994) The toxicokinetics and metabolism of polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) and their relevance for toxicity. Crit Rev Toxicol 24:1–74CrossRefGoogle Scholar
  45. Van den Berg M, Birnbaum L, Bosveld ATC, Brunström B, Cook P, Feeley M, Giesy JP, Hanberg A, Hasegawa R, Kennedy SW, Kubiak T, Larsen JC, van Leeuwen FXR, Liem AKD, Nolt C, Peterson RE, Poellinger L, Safe S, Schrenk D, Tillitt D, Tysklind M, Younes M, Waern F, Zacharewski T (1998) Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ Health Perspect 106:775–792CrossRefGoogle Scholar
  46. Van den Berg M, Birnbaum LS, Denison M, De Vito M, Farland W, Feeley M, Fiedler H, Hakansson H, Hanberg A, Haws L, Rose M, Safe S, Schrenk D, Tohyama C, Tritscher A, Tuomisto J, Tysklind M, Walter N, Peterson RE (2006) The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 93:223–241CrossRefGoogle Scholar
  47. Wren CD, Hunter DB, Leatherland JF, Stokes PM (1987a) The effects of polychlorinated biphenyls and methylmercury, singly and in combination on mink. II: Reproduction and kit development. Arch Environ Contam Toxicol 16:449–454CrossRefGoogle Scholar
  48. Wren CD, Hunter DB, Leatherland JF, Stokes PM (1987b) The effects of polychlorinated biphenyls and methylmercury, singly and in combination on mink. I: Uptake and toxic responses. Arch Environ Contam Toxicol 16:441–447CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.ENVIRON International CorpBurtonUSA
  2. 2.ENVIRON International Corp.PortlandUSA

Personalised recommendations