2,3,7,8-Tetrachlorodibenzo-p-dioxin equivalents in tissues of birds at Green Bay, Wisconsin, USA

  • Paul D. Jones
  • John P. Giesy
  • John L. Newsted
  • David A. Verbrugge
  • Donald L. Beaver
  • Gerald T. Ankley
  • Donald E. Tillitt
  • Keith B. Lodge
  • Gerald J. Niemi


The environment has become contaminated with complex mixtures of planar, chlorinated hydrocarbons (PCHs) such as polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs) and structurally similar compounds. Because the potencies of individual congeners to cause the same adverse effects vary greatly and the relative as well as absolute concentrations of individual PCH vary among samples from different locations, it is difficult to assess the toxic effects of these mixtures on wildlife. These compounds can cause a number of adverse effects, however, because the toxic effects which occur at ecologically-relevant concentrations such as embryo-lethality and birth defects appear to be mediated through the same mechanism, the potency of individual congeners can be reported relative to 2,3,7,8-tetrachlorodibenzo-p-dioxin (2,3,7,8-TCDD) which is the most toxic congener in the PCH class. The concentations of 2,3,7,8-TCDD Equivalents (TCDD-EQ) were determined in the tissues of aquatic and terrestrial birds of Green Bay, Wisconsin by the H4IIE bioassay system and compared toxic equivalency factors (TEFs) with the concentration predicted by the use of toxic equivalency factors applied to concentrations of PCH, which were determined by instrumental analyses. Concentrations of TCDD-EQ ranged from 0.52 to 440 ng/kg, wet weight. The greatest concentrations occurred in the fish-eating birds. Concentrations of TCDD-EQ, which were determined by the two methods were significantly correlated, but the additive model which used the TEFs with concentrations of measured PCB, PCDD and PCDF congeners underestimated the concentrations of TCDD-EQ measured by the H4IIE bioassay by an average of 57%. This is thought to be due to contributions from un-quantified PCH, which are known to occur in the environment. Of the quantified PCH congeners, PCDD and PCDF contributed a small portion of the TCDD-EQ in the aquatic birds, while most of the TCDD-EQ were due to non-ortho-substituted PCBs. In the terrestrial birds, the proportion of the TCDD-EQ contributed by the PCDD and PCDF was greater.


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  1. Addison RF, Hansen PD, Pluta HJ, Willis DE (1991) Effects of Ugilec-141, a PCB substitute based on tetrachlorobenzyltoluenes, on hepatic mono-oxygenase induction in estuarine fish. Mar Environ Res 31:137–144Google Scholar
  2. Addison RF, Zink ME, Willis DE, Wrench JJ (1982) Induction of hepatic mixed function oxidase activity in trout (Salvelinus fontinalis) by Aroclor® 1254 and some aromatic hydrocarbon replacements. Toxicol Appl Pharm 63:166–172Google Scholar
  3. Ankley GT, Niemi GJ, Lodge KB, Harris HJ, Beaver DL, Jones PD, Giesy JP, Tillitt DE, Schwartz TR, Hagley C (1993) Bioaccumulation of planar, polychlorinated dibenzo furans and dibenzo-p-dioxins by birds nesting in the lower Fox River and Green Bay, Wisconsin, USA. Arch Environ Contam Toxicol 24:332–344.Google Scholar
  4. Bannister R, Safe S (1987) The effects of receptor antagonists on the AHH induction activity of 2,3,7,8-TCDD in C57BL/6 and DBA/2 mice: 1,3,6,8-Tetrachlorodibenzofuran. Chemosphere 16:1739–1742Google Scholar
  5. Bauman PC, Whittle DM (1988) The status of selected organics in the Laurentian Great Lakes: An overview of DDT, PCBs, dioxins, furans and aromatic hydrocarbons. Aquat Toxicol 11:241–257.Google Scholar
  6. Becker M, Phillips T, Safe S (1991) Polychlorinated diphenyl ethers—A review. Toxicol Environ Chem 33:189–200Google Scholar
  7. Birnbaum LS (1985) The role of structure in the disposition of halogenated aromatic xenobiotics. Environ Health Perspect 61:11–20Google Scholar
  8. Boon JP, Eijgenraam F, Everaats JM, Duinker JC (1989) A structureactivity relationship (SAR) approach towards metabolism of PCBs in marine animals from different trophic levels. Marine Environ Res 27:159–176Google Scholar
  9. Borlakoglu JT, Wilkins JPG, Walker CH (1988) Polychlorinated biphenyls in fish-eating sea birds- Molecular features and metabolic interpretations. Marine Environ Res 24:15–19Google Scholar
  10. Bradlaw JA, Casterline JL (1979). Induction of enzymes in cell cultures: a rapid screen for the detection of planar chlorinated organic compounds. J Assoc Offic Anal Chem 62:904–916Google Scholar
  11. Broman D, Näf, Rolff C, Zebühr Y, Fry B, Hobbie J (1992) Using ratios of stable nitrogen isotopes to estimate bioaccumulation and flux of polychlorinated dibenzo-p-dioxins (PCDDs) in two food chains from the northern Baltic. Environ Toxicol Chem 11:331–345Google Scholar
  12. Brunström B (1990) Toxicity of coplanar polychlorinated biphenyls in avian embryos. Arch Toxicol 64:188–192Google Scholar
  13. Brunström B, Broman D, Dencker L, Näf C, Vejlens E, Zebür Y (1992) Extracts from settling particulate matter collected in the Stockholm Archepeliga waters: Embryolethality, immunoaromatics, diaromatics or polyaromatics. Environ Toxicol Chem 11:1441–1449Google Scholar
  14. Buser HR, Kjeller LO, Swanson SE, Rappe C (1986) Methyl-, polymethyl and alkylpolychlorodibenzofurans identified in pulp mill sludge and sediments. Environ Sci Technol 20:404–408Google Scholar
  15. Chui YC, Addison RF, Law FCP (1990) Acute toxicity and toxicokinetics of chlorinated diphenyl ethers in trout. Xenobiotica 20:489–499Google Scholar
  16. Chui YC, Hansell MM, Addison RF, Law FCP (1985) Effects of chlorinated diphenyl ethers on the mixed-function oxidases and ultrastructure of rat and trout liver. Toxicol Appl Pharm 81:287–294Google Scholar
  17. Custer TW, Bunck CM, Stafford CJ (1985) Organochlorine concentrations in pre-fledging common terns at three Rhode Island colonies. Colon Water Birds 8:150–153.Google Scholar
  18. De Voogt P, Brinkman UATh (1989) Production, properties and usage of polychlorinated biphenyls. In Kimbrough RD, Jensen AA (eds) Halogenated biphenyls, terphenyls, napthalenes, Dibenzo-p-dioxins and related products. Elsevier Science Publishers BV, Amsterdam, pp 3–45Google Scholar
  19. De Voogt P, Wegener JWM, Klamer JC, Van Zijl GA, and Govers H (1988) Prediction of environmental fate and effects of heteroatomic polycyclic aromatics by QSARS: The position of n-octanol/water partition coefficients. Biomed Environ Sci 1:194–209Google Scholar
  20. De Voogt P, Wells DE, Reutergardh L, Brinkman UATh (1990) Biological activity, determination and occurrence of planar, monoand di-ortho PCBs. Int J Environ Chem 40:1–46Google Scholar
  21. Denison MS, Fisher JM, Whitlock JP (1989) Protein-DNA interactions at recognition sites for the dioxin-Ah receptor complex. J Biol Chem 264:16478–16482Google Scholar
  22. Finney DJ (1978) Statistical Methods in Biological Assays, 3rd ed. Charles Griffin and Company, Ltd, London, 333 ppGoogle Scholar
  23. Fox GA, Collins B, Hayakawa E, Weseloh DV, Ludwig JP, Kubiak TJ, Erdman TC (1991a) Reproductive outcomes in colonial fisheating birds: A biomarker for developmental toxicants in Great Lakes food chains. II. Spatial variation in the occurrence and prevalence of bill defects in young double-crested cormorants in the Great Lakes, 1979–1987. J Great Lakes Res 17:158–167Google Scholar
  24. Fox GA, Weseloh DV, Kubiak TJ, Erdman TC (1991b) Reproductive outcomes in colonial fish-eating birds: A biomarker for developmental toxicants in Great Lakes food chains. I. Historical and ecotoxicological perspectives J Great Lakes Res 17:153–157Google Scholar
  25. Fox GA, Gilbertson M, Gillman AP, Kubiak TJ (1991c) A rationale for the use of colonial fish-eating birds to monitor the persistence of developmental toxicants in Great Lakes fish. J Great Lakes Res 17:151–152Google Scholar
  26. Goldstein JA (1980) Structure-activity relationships for the biochemical effects and the relationship to toxicity. In: Kimbrough RD, Jensen AA (eds) Halogenated biphenyls, terphenyls napthalenes, dibenzo-p-dioxins and related products, vol 4—Topics in environmental health, 1st ed. Elsevier, Amsterdam, pp 151–190Google Scholar
  27. Gonzalez FJ, Tukey RH, Nebert DW (1984) Structural gene products of the Ah locus. Transcriptional regulation of cytochrome P1-450 and P3-450 mRNA levels by 3-methylcholanthrine. Mol Pharmacol 26:117–121Google Scholar
  28. Haas CN, Schett PA (1990) Estimation of averages in truncated samples. Environ Sci Technol 24:912–919Google Scholar
  29. Haglund P, Egebäck KE, Jansson B (1988) Analysis of polybrominated dioxins and furans in vehicle exhaust Chemosphere 17:2129–2140Google Scholar
  30. Hilker DR, Aldous KM, Smith RM, O'Keefe PW, Gierthy JF, Jurusik J, Hibbons SW, Spink D, Parillo RJ (1985) Detection of sulfur analog of 2,3,7,8-TCDD in the environment Chemosphere 14:1275–1284Google Scholar
  31. Howie L, Dickerson R, Davis D, Safe S (1990) Immunosuppressive and monooxygenase induction activities of polychlorinated diphenyl ether congeners in C57BL/6N mice: Quantitative structureactivity relationships. Toxicol Appl Pharm 105:254Google Scholar
  32. Jansson B, Jensen S, Olsson M, Renberg M, Sundströmand L, Vaz R (1975) Identification by GC-MS of phenolic metabolites of PCB andp,p′-DDE isolated from Baltic guillemot and seal. Ambio 4:93–97Google Scholar
  33. Kannan N, Tanabe S, Wakimoto T, Tatsukawa R (1987). Coplanar polychlorinated biphenyls in Aroclor and Kanechlor mixtures. J Off Assoc Anal Chem 70:451–454Google Scholar
  34. Kannan N, Tanabe S, Tatsukawa R (1988) Toxic potential of nonortho and mono-ortho coplanar PCBs in commercial PCB preparations: 2,3,7,8-T4 CDD toxicity equivalence factors approach. Bull Env Contain Toxicol 41:267–276Google Scholar
  35. Kubiak TJ, Harris HJ, Smith LM, Schwartz TR, Stalling DL, Trick JA, Sileo L, Docherty DE, Erdman TC (1989) Micrcontaminants and reproductive impairment of the Forster's Tern on Green Bay, Lake Michigan—1983. Arch Environ Contain Toxicol 18:706–727Google Scholar
  36. Kuehl DW, Butterworth BC, Libal J, Marquis P (1991) An isotope dilution high resolution mass spectrometric method for the determination of coplanar polychlorinated biphenyls: Application to fish and marine mammals. Chemosphere 22:849–858Google Scholar
  37. Lake JL, Rogerson PF, Norwood CB (1981) A polychlorinated dibenzofuran and related compounds in an estuarine ecosystem. Environ Sci Technol 15:549–553Google Scholar
  38. McConnell EE (1989) Acute and chronic toxicity and carcinogenesis in animals. In: Kimbrough RD, Jensen AA (eds) Halogenated biphenyls, terphenyls, napthalenes, dibenzo-p-dioxins and related products. Elsevier Science Publishers BV, Amsterdam, pp 161–193Google Scholar
  39. McFarland VA, Clarke JU (1989) Environmental occurrence, abundance, and potential toxicity of polychlorinated biphenyl congeners: Considerations for a congener-specific analysis. Environ Health Perspect 81:225–239Google Scholar
  40. McKinney JD, Fawkes J, Jordan S, Chae K, Oatley S, Coleman RE, Briner W (1985) 2,3,7,8-Tetrachlorodibenozo-p-dioxin (TCDD) as a potent and persistent thyroxine agonist: A mechanistic model for toxicity based on molecular reactivity. Environ Health Perspect 61:41–53Google Scholar
  41. Morrissey RE, Schwetz BA (1989) Reproductive and developmental toxicity in animals. In: Kimbrough RD, Jensen AA (eds) Halogenated biphenyls, terphenyls, napthalenes, dibenzo-p-dioxins and Related Products. Elsevier Science Publishers BV, Amsterdam, pp 195–225Google Scholar
  42. Muir DCG, Norstrom RJ, Simon M (1988) Organochlorine contaminants in arctic marine food chains: Accumulation of specific polychlorinated biphenyls and chlordane-related compounds. Environ Sci Technol 22:1071–1079Google Scholar
  43. Murk AJ, van den Berg JHJ, Koeman JH, Brouwer A (1991) The toxicity of tetrachlorobenzyltoluenes (Ugilec 141) and polychloro-biphenyls (Aroclor 1254 and PCB-77) compared inAh-responsive andAh-nonresponsive mice. Environ Pollut 77:57–67Google Scholar
  44. Nebert DW (1990) TheAh locus: Genetic differences in toxicity, cancer, mutation, and birth defects. Crit Rev Toxicol 20:153–174Google Scholar
  45. Nevalainen T, Koistinen J (1991) Model compound synthesis for the structure determination of new unknown planar aromatic compounds originating from pulp mill. Chemosphere 23:1581–1589Google Scholar
  46. Norstrom RJ (1987) Bioaccumulation of polychlorinated biphenyls in Canadian wildlife. In: Hazards, decontamination and replacement of PCBs. Plenum Publishing, NY, pp 1–16Google Scholar
  47. Norstrom RJ, Simon M, Muir DCG, Schweinberg RE (1988) Organochlorine contaminants in arctic food chains: Identification, geographical distribution, and temporal trends in polar bears. Environ Sci Technol 22:1063–1071Google Scholar
  48. Parkinson A, Safe S (1987) Mammalian biologic and toxic effects of PCBs. In: Safe S, Hutzinger O (eds) Polychlorinated biphenyls (PCBs): Mammalian and environmental toxicology. Springer-Verlag, Berlin, pp 49–75Google Scholar
  49. Poland A, Knutson C (1982) 2,3,7,8-Tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: Examination of the mechanism of toxicity. Ann Rev Pharmacol Toxicol 22:517–554Google Scholar
  50. Pratt RM (1985) Receptor-dependent mechanisms of glucocorticoid and dioxin-induced cleft plate. Environ Health Perspect 61:35–40Google Scholar
  51. Pruell RJ, Bowen, RD, Fluck SJ, LiVosi JA, Cobb DJ, Lake JL (1988) PCB congeners in American lobster,Homarus americanus and winter flounder,Pseudopleuronectes americanus, from New Bedford Harbor, Massachusetts. USEPA Environmental Assessment Group Report, Washington, DCGoogle Scholar
  52. Ribick MA, Smith LM, Dubay GR, Stalling DL (1981) Applications and results of analytical methods used in monitoring environmental contaminants. In: Branson DR, Dickson, KL (Eds) Aquatic Toxicology and Hazard Assessment; ASTM STP 737; Philadelphia, PA; pp 249–269Google Scholar
  53. Safe S (1990) Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: Environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Crit Rev Toxicol 21:51–88Google Scholar
  54. Sawyer TW, Vatcher AD, Safe S (1984) Comparative aryl hydrocarbon hydroxylase induction activities of commercial PCBs in Wistar rats and rat hepatoma H-4-II-E cells in culture. Chemosphere 13:695–701Google Scholar
  55. Sellström U, Jansson B, Nylund K, Odsjö Y, Olsson M (1990) Anthropogenic brominated aromatics in the Swedish Environment. Chlorinated Benzenes and Related Compounds 2:357–360Google Scholar
  56. Sijm DTHM, Yarechewski AL, Muir DCG, Webster GRB, Seinen W, Opperhuizen A (1990) Biotransformation and tissue distribution of 1,2,3,7-tetrachlorodmibenzo-p-dioxin, 1,2,3,4,7-pentachlorodibenzo-p-dioxin and 2,3,4,7,8-pentachlorodibenzofuran in rainbow trout. Chemosphere 21:845–866Google Scholar
  57. Silkworth JB, Cutler DS, Sack G (1989). Immunotoxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in a complex environmental mixture from the Love Canal. Fundam Appl Toxicol 12:303–312Google Scholar
  58. Smith LM, Schwartz TR, Feltz K, Kubiak T (1990) Determination and occurrence of AHH-active polychlorinated biphenyls, 2,3,7,8-tetrachloro-p-dioxin and 2,3,7,8-tetrachlorodibenzofuran in Lake Michigan sediment and biota. The question of their relative toxicological significance. Chemosphere 21:1063–1085Google Scholar
  59. Stafford CJ (1983) Halogenated diphenyl ethers identified in avian tissues and eggs by GC-MS. Chemosphere 12:1487–1495Google Scholar
  60. Sundström G, Hutzinger O (1976) The synthesis of chlorinated diphenyl ethers. Chemosphere 5:305–312Google Scholar
  61. Tanabe S, Kannan N, Subramanian A, Watanabe S, Tatsukawa R (1987) Highly toxic coplanar PCBs: occurrence, source, persistency and toxic implications to wildlife and humans. Environ Pollut 47:147–163Google Scholar
  62. Tanabe S, Kannan N, Fukushima M, Okamoto T, Wakimoto T, Tatsukawa R (1989a) Persistent organochlorines in Japanese coastal waters: An introspective summary from a far east developed nation. Marine Pollut Bull 20:344–352Google Scholar
  63. Tanabe S, Kannan N, Wakimoto T, Tatsukawa R, Okamoto T, Masuda Y (1989b). Isomer-specific determination and toxic evaluation of potentially hazardous coplanar PCBs, dibenzofurans and dioxins in the tissues of “Yusho” PCB poisoning victim and in the causal oil. Toxicol Environ Chem 24:215–231Google Scholar
  64. Tillitt DE, Giesy JP, Ankley GT (1991a). Characterization of the H4IIE rat hepatoma cell bioassay as a tool for assessing toxic potency of planar halogenated hydrocarbons in environmental samples. Environ Sci Technol 25:87–92Google Scholar
  65. Tillitt DE, Ankley GT, Verbrugge D, Giesy JP (1991b) H41IE rat hepatoma cell bioassay-derived 2,3,7,8-tetrachlordibenzo-p-di-oxin equivalents in colonial fish-eating waterbird eggs from the Great Lakes. Arch Environ Contamn Toxicol 21:91–101Google Scholar
  66. Tillitt DE, Giesy JP, Ludwig JP, Kurita-Matsuba H, Weseloh DV, Ross PS, Bishop CA, Sileo L, Stromberg K, Larson J, Kubiak TJ (1992) Polychlorinated biphenyl residues and egg mortality in double-crested cormorants from the Great Lakes. Environ Toxicol Chem 11:1281–1288Google Scholar
  67. U.S. Environmental Protection Agency (1990b) Analytical procedures and quality assurance plan for the determination of PCDD/PCDF in fish. EPA/600/3-90/022. U.S. Environmental Protection Agency, Duluth, MNGoogle Scholar
  68. (1990a) Analytical procedures and quality assurance plan for the determination of xenobiotic chemical contaminants in fish. EPA/600/3-90/023. U.S. Environmental Protection Agency, Duluth, MNGoogle Scholar
  69. Walker CH (1990) Persistent pollutants in fish-eating sea birds-bioaccumulation, metabolism and effects. Aquat Toxicol 17:293–324Google Scholar
  70. Williams LL, Giesy JP, DeGalan N, Verbrugge DA, Tillitt DE, Ankley GT, Welch RA (1991) Prediction of concentrations of 2,3,7,8-TCDD equivalents (TCDD-EQ) in trimmed, chinook salmon filletts from Lake Michigan from total concentrations of PCBs and fish size. Environ Sci Techniol (in press).Google Scholar
  71. Zacharewski T, Harris T, Safe S, Thoma H, Hutzinger O (1988) Applications of thein vitro aryl hydrocarbon hydroxylase induction assay for determining “2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents”. Pyrolyzed brominated flame retardants. Toxicology 51:177–189Google Scholar
  72. Zacharewski T, Safe L, Safe S, Chittim B, DeVault D, Wiberg K, Berquist PA, Rappe C (1989). Comparative analysis of polychlorinated dibenzo-p-dioxin and dibenzofuran congeners in Great Lakes fish extracts by gas chromatography-mass spectrometry and in vitro enzyme induction activities. Environ Sci Technol 23:730–735Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1993

Authors and Affiliations

  • Paul D. Jones
    • 1
  • John P. Giesy
    • 1
  • John L. Newsted
    • 1
  • David A. Verbrugge
    • 1
  • Donald L. Beaver
    • 2
  • Gerald T. Ankley
    • 3
  • Donald E. Tillitt
    • 4
  • Keith B. Lodge
    • 5
  • Gerald J. Niemi
    • 5
  1. 1.Department of Fisheries and Wildlife, Pesticide Research Center and Institute for Environmental ToxicologyMichigan State UniversityEast LansingUSA
  2. 2.Department of ZoologyMichigan State UniversityEast LansingUSA
  3. 3.Environmental Research Laboratory-DuluthUS-EPADuluthUSA
  4. 4.U.S. Fish and Wildlife ServiceNational Fisheries Contaminant Research CenterColumbiaUSA
  5. 5.Natural Resources Research InstituteUniversity of Minnesota-DuluthDuluthUSA
  6. 6.DSIR ChemistryGracefield Research Center, Private BagLower HuttNew Zeland

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