Skip to main content
Log in

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

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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 31:137–144

    Google Scholar 

  • 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 63:166–172

    Google Scholar 

  • 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 

  • 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 16:1739–1742

    Google Scholar 

  • 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 

  • Becker M, Phillips T, Safe S (1991) Polychlorinated diphenyl ethers—A review. Toxicol Environ Chem 33:189–200

    Google Scholar 

  • Birnbaum LS (1985) The role of structure in the disposition of halogenated aromatic xenobiotics. Environ Health Perspect 61:11–20

    Google Scholar 

  • 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 27:159–176

    Google Scholar 

  • Borlakoglu JT, Wilkins JPG, Walker CH (1988) Polychlorinated biphenyls in fish-eating sea birds- Molecular features and metabolic interpretations. Marine Environ Res 24:15–19

    Google Scholar 

  • 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 62:904–916

    Google Scholar 

  • 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 11:331–345

    Google Scholar 

  • Brunström B (1990) Toxicity of coplanar polychlorinated biphenyls in avian embryos. Arch Toxicol 64:188–192

    Google Scholar 

  • 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 11:1441–1449

    Google Scholar 

  • Buser HR, Kjeller LO, Swanson SE, Rappe C (1986) Methyl-, polymethyl and alkylpolychlorodibenzofurans identified in pulp mill sludge and sediments. Environ Sci Technol 20:404–408

    Google Scholar 

  • Chui YC, Addison RF, Law FCP (1990) Acute toxicity and toxicokinetics of chlorinated diphenyl ethers in trout. Xenobiotica 20:489–499

    Google Scholar 

  • 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 81:287–294

    Google Scholar 

  • 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 

  • 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 3–45

    Google Scholar 

  • 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 1:194–209

    Google Scholar 

  • 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 40:1–46

    Google Scholar 

  • Denison MS, Fisher JM, Whitlock JP (1989) Protein-DNA interactions at recognition sites for the dioxin-Ah receptor complex. J Biol Chem 264:16478–16482

    Google Scholar 

  • Finney DJ (1978) Statistical Methods in Biological Assays, 3rd ed. Charles Griffin and Company, Ltd, London, 333 pp

    Google Scholar 

  • 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 17:158–167

    Google Scholar 

  • 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 17:153–157

    Google Scholar 

  • 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 17:151–152

    Google Scholar 

  • 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 151–190

    Google Scholar 

  • 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 26:117–121

    Google Scholar 

  • Haas CN, Schett PA (1990) Estimation of averages in truncated samples. Environ Sci Technol 24:912–919

    Google Scholar 

  • Haglund P, Egebäck KE, Jansson B (1988) Analysis of polybrominated dioxins and furans in vehicle exhaust Chemosphere 17:2129–2140

    Google Scholar 

  • 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 14:1275–1284

    Google Scholar 

  • 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 105:254

    Google Scholar 

  • 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 4:93–97

    Google Scholar 

  • Kannan N, Tanabe S, Wakimoto T, Tatsukawa R (1987). Coplanar polychlorinated biphenyls in Aroclor and Kanechlor mixtures. J Off Assoc Anal Chem 70:451–454

    Google Scholar 

  • 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 41:267–276

    Google Scholar 

  • 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 18:706–727

    Google Scholar 

  • 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 22:849–858

    Google Scholar 

  • Lake JL, Rogerson PF, Norwood CB (1981) A polychlorinated dibenzofuran and related compounds in an estuarine ecosystem. Environ Sci Technol 15:549–553

    Google Scholar 

  • 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 161–193

    Google Scholar 

  • McFarland VA, Clarke JU (1989) Environmental occurrence, abundance, and potential toxicity of polychlorinated biphenyl congeners: Considerations for a congener-specific analysis. Environ Health Perspect 81:225–239

    Google Scholar 

  • 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 61:41–53

    Google Scholar 

  • 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 195–225

    Google Scholar 

  • 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 22:1071–1079

    Google Scholar 

  • 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 77:57–67

    Google Scholar 

  • Nebert DW (1990) TheAh locus: Genetic differences in toxicity, cancer, mutation, and birth defects. Crit Rev Toxicol 20:153–174

    Google Scholar 

  • Nevalainen T, Koistinen J (1991) Model compound synthesis for the structure determination of new unknown planar aromatic compounds originating from pulp mill. Chemosphere 23:1581–1589

    Google Scholar 

  • Norstrom RJ (1987) Bioaccumulation of polychlorinated biphenyls in Canadian wildlife. In: Hazards, decontamination and replacement of PCBs. Plenum Publishing, NY, pp 1–16

    Google Scholar 

  • 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 22:1063–1071

    Google Scholar 

  • 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 49–75

    Google Scholar 

  • 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 22:517–554

    Google Scholar 

  • Pratt RM (1985) Receptor-dependent mechanisms of glucocorticoid and dioxin-induced cleft plate. Environ Health Perspect 61:35–40

    Google Scholar 

  • 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, DC

  • 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 249–269

  • 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 21:51–88

    Google Scholar 

  • 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 13:695–701

    Google Scholar 

  • Sellström U, Jansson B, Nylund K, Odsjö Y, Olsson M (1990) Anthropogenic brominated aromatics in the Swedish Environment. Chlorinated Benzenes and Related Compounds 2:357–360

    Google Scholar 

  • 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 21:845–866

    Google Scholar 

  • 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 12:303–312

    Google Scholar 

  • 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 21:1063–1085

    Google Scholar 

  • Stafford CJ (1983) Halogenated diphenyl ethers identified in avian tissues and eggs by GC-MS. Chemosphere 12:1487–1495

    Google Scholar 

  • Sundström G, Hutzinger O (1976) The synthesis of chlorinated diphenyl ethers. Chemosphere 5:305–312

    Google Scholar 

  • 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 47:147–163

    Google Scholar 

  • 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 20:344–352

    Google Scholar 

  • 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 24:215–231

    Google Scholar 

  • 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 25:87–92

    Google Scholar 

  • 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 21:91–101

    Google Scholar 

  • 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 11:1281–1288

    Google Scholar 

  • 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, MN

    Google Scholar 

  • (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, MN

    Google Scholar 

  • Walker CH (1990) Persistent pollutants in fish-eating sea birds-bioaccumulation, metabolism and effects. Aquat Toxicol 17:293–324

    Google Scholar 

  • 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).

  • 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 51:177–189

    Google Scholar 

  • 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 23:730–735

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This paper has been reviewed in accord with U.S. Environmental Protection Agency policy. Mention of specific products or trade names does not imply endorsement by the U.S. Government.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jones, P.D., Giesy, J.P., Newsted, J.L. et al. 2,3,7,8-Tetrachlorodibenzo-p-dioxin equivalents in tissues of birds at Green Bay, Wisconsin, USA. Arch. Environ. Contam. Toxicol. 24, 345–354 (1993). https://doi.org/10.1007/BF01128732

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01128732

Keywords

Navigation