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. 2004 Apr;112(5):532–537. doi: 10.1289/ehp.6756

Effects of organochlorine contaminants on thyroid hormone levels in Arctic breeding glaucous gulls, Larus hyperboreus.

Jonathan Verreault 1, Janneche Utne Skaare 1, Bjørn Munro Jenssen 1, Geir Wing Gabrielsen 1
PMCID: PMC1241916  PMID: 15064156

Abstract

Studies on glaucous gulls (Larus hyperboreus) breeding in the Barents Sea have reported that high blood levels of halogenated organic contaminants in this species might cause reproductive, behavioral, and developmental stress. However, potential endocrine system modulation caused by contaminant exposure has yet not been reported in this Arctic apical predator. In this present study we aimed to investigate whether the current levels of a selection of organochlorines (OCs) were associated with altered circulating levels of thyroid hormones (THs) in free-ranging adult glaucous gulls breeding at Bear Island in the Barents Sea. Blood concentrations of 14 polychlorinated biphenyls, hexachlorobenzene (HCB), oxychlordane, and p,p' -dichlorodiphenyldichloroethylene (p,p' -DDE) were quantified, in addition to free and total thyroxine (T4) and triiodothyronine (T3), in plasma of 66 glaucous gulls in the spring of 2001. Negative correlations were found between plasma levels of T4 and T4:T3 ratio, and blood levels of OCs in male glaucous gulls. Despite their relatively low contribution to the total OC fraction, HCB and oxychlordane were the most prominent compounds in terms of their negative effect on the variation of the T4:T3 ratio. Moreover, lower T4 levels and T4:T3 ratios were measured in glaucous gulls breeding in a colony exposed to high levels of OCs, compared with a less exposed colony. Levels of T3 were elevated in the high-OC-exposed colony. This may indicate that the glaucous gull is susceptible to changes to TH homeostasis mediated by exposure to halogenated organic contaminants.

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Selected References

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  1. Bargar T. A., Scott G. I., Cobb G. P. Maternal transfer of contaminants: case study of the excretion of three polychlorinated biphenyl congeners and technical-grade endosulfan into eggs by white Leghorn chickens (Gallus domesticus). Environ Toxicol Chem. 2001 Jan;20(1):61–67. [PubMed] [Google Scholar]
  2. Bernhoft A., Wiig Ø, Skaare J. U. Organochlorines in polar bears (Ursus maritimus) at Svalbard. Environ Pollut. 1997;95(2):159–175. doi: 10.1016/s0269-7491(96)00122-4. [DOI] [PubMed] [Google Scholar]
  3. Borgå K., Gabrielsen G. W., Skaare J. U. Biomagnification of organochlorines along a Barents Sea food chain. Environ Pollut. 2001;113(2):187–198. doi: 10.1016/s0269-7491(00)00171-8. [DOI] [PubMed] [Google Scholar]
  4. Brevik E. M. Gas chromatograhic method for the determination of organochlorine pesticides in human milk. Bull Environ Contam Toxicol. 1978 Mar;19(3):281–286. doi: 10.1007/BF01685799. [DOI] [PubMed] [Google Scholar]
  5. Brouwer A. Inhibition of thyroid hormone transport in plasma of rats by polychlorinated biphenyls. Arch Toxicol Suppl. 1989;13:440–445. doi: 10.1007/978-3-642-74117-3_87. [DOI] [PubMed] [Google Scholar]
  6. Brouwer A., Morse D. C., Lans M. C., Schuur A. G., Murk A. J., Klasson-Wehler E., Bergman A., Visser T. J. Interactions of persistent environmental organohalogens with the thyroid hormone system: mechanisms and possible consequences for animal and human health. Toxicol Ind Health. 1998 Jan-Apr;14(1-2):59–84. doi: 10.1177/074823379801400107. [DOI] [PubMed] [Google Scholar]
  7. Brouwer A., van den Berg K. J. Binding of a metabolite of 3,4,3',4'-tetrachlorobiphenyl to transthyretin reduces serum vitamin A transport by inhibiting the formation of the protein complex carrying both retinol and thyroxin. Toxicol Appl Pharmacol. 1986 Sep 30;85(3):301–312. doi: 10.1016/0041-008x(86)90337-6. [DOI] [PubMed] [Google Scholar]
  8. Bustnes Jan Ove, Bakken Vidar, Skaare Janneche Utne, Erikstad Kjell Einar. Age and accumulation of persistent organochlorines: a study of Arctic-breeding glaucous gulls (Larus hyperboreus). Environ Toxicol Chem. 2003 Sep;22(9):2173–2179. doi: 10.1897/02-456. [DOI] [PubMed] [Google Scholar]
  9. Davison T. F., Flack I. H., Butler E. J. The binding of thyroxine and tri-iodothyronine to plasma proteins in the chicken at the physiological pH. Res Vet Sci. 1978 Nov;25(3):280–283. [PubMed] [Google Scholar]
  10. Henriksen E. O., Gabrielsen G. W., Trudeau S., Wolkers J., Sagerup K., Skaare J. U. Organochlorines and possible biochemical effects in glaucous gulls (Larus hyperboreus) from Bjørnøya, the Barents Sea. Arch Environ Contam Toxicol. 2000 Feb;38(2):234–243. doi: 10.1007/s002449910031. [DOI] [PubMed] [Google Scholar]
  11. Ingebrigtsen K., Skaare J. U., Teigen S. W. Organochlorine residues in two Norwegian puffin (Fratercula arctica) colonies. J Toxicol Environ Health. 1984;14(5-6):813–828. doi: 10.1080/15287398409530629. [DOI] [PubMed] [Google Scholar]
  12. Kleiman de Pisarev D. L., Rios de Molina M. C., San Martin de Viale L. C. Thyroid function and thyroxine metabolism in hexachlorobenzene-induced porphyria. Biochem Pharmacol. 1990 Mar 1;39(5):817–825. doi: 10.1016/0006-2952(90)90195-q. [DOI] [PubMed] [Google Scholar]
  13. Lans M. C., Spiertz C., Brouwer A., Koeman J. H. Different competition of thyroxine binding to transthyretin and thyroxine-binding globulin by hydroxy-PCBs, PCDDs and PCDFs. Eur J Pharmacol. 1994 Apr 4;270(2-3):129–136. doi: 10.1016/0926-6917(94)90054-x. [DOI] [PubMed] [Google Scholar]
  14. McNabb F. M. Anne, Fox Glen A. Avian thyroid development in chemically contaminated environments: is there evidence of alterations in thyroid function and development? Evol Dev. 2003 Jan-Feb;5(1):76–82. doi: 10.1046/j.1525-142x.2003.03012.x. [DOI] [PubMed] [Google Scholar]
  15. Moccia R. D., Fox G. A., Britton A. A quantitative assessment of thyroid histopathology of herring gulls (Larus argentatus) from the Great Lakes and a hypothesis on the causal role of environmental contaminants. J Wildl Dis. 1986 Jan;22(1):60–70. doi: 10.7589/0090-3558-22.1.60. [DOI] [PubMed] [Google Scholar]
  16. Refetoff S., Robin N. I., Fang V. S. Parameters of thyroid function in serum of 16 selected vertebrate species: a study of PBI, serum T4, free T4, and the pattern of T4 and T3 binding to serum proteins. Endocrinology. 1970 Apr;86(4):793–805. doi: 10.1210/endo-86-4-793. [DOI] [PubMed] [Google Scholar]
  17. Rolland R. M. A review of chemically-induced alterations in thyroid and vitamin A status from field studies of wildlife and fish. J Wildl Dis. 2000 Oct;36(4):615–635. doi: 10.7589/0090-3558-36.4.615. [DOI] [PubMed] [Google Scholar]
  18. Rothman K. J. No adjustments are needed for multiple comparisons. Epidemiology. 1990 Jan;1(1):43–46. [PubMed] [Google Scholar]
  19. Sagerup Kjetil, Henriksen Espen O., Skaare Janneche U., Gabrielsen Geir W. Intraspecific variation in trophic feeding levels and organochlorine concentrations in glaucous gulls (Larus hyperboreus) from Bjørnøya, the Barents Sea. Ecotoxicology. 2002 Apr;11(2):119–125. doi: 10.1023/a:1014473012572. [DOI] [PubMed] [Google Scholar]
  20. Tanabe Shinsuke. Contamination and toxic effects of persistent endocrine disrupters in marine mammals and birds. Mar Pollut Bull. 2002;45(1-12):69–77. doi: 10.1016/s0025-326x(02)00175-3. [DOI] [PubMed] [Google Scholar]
  21. Van den Berg K. J., van Raaij J. A., Bragt P. C., Notten W. R. Interactions of halogenated industrial chemicals with transthyretin and effects on thyroid hormone levels in vivo. Arch Toxicol. 1991;65(1):15–19. doi: 10.1007/BF01973497. [DOI] [PubMed] [Google Scholar]
  22. Vos J. G., Dybing E., Greim H. A., Ladefoged O., Lambré C., Tarazona J. V., Brandt I., Vethaak A. D. Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation. Crit Rev Toxicol. 2000 Jan;30(1):71–133. doi: 10.1080/10408440091159176. [DOI] [PubMed] [Google Scholar]

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