Chronic dietary exposure to environmental organochlorine contaminants induces thyroid gland lesions in Arctic foxes (Vulpes lagopus)

Environmental Research

Volumn 109, Issue 6, 2009, Pages 702-711

  Sonne, Christian ^a   Wolkers, Hans ^b   Leifsson, Pall S ^c   Iburg, Tine ^c   Jenssen, Bjørn Munro ^d   Fuglei, Eva ^b   Ahlstrøm, Øystein ^e   Dietz, Rune ^a   Kirkegaard, Maja ^a   Muir, Derek C G ^f   Jørgensen, Even H ^g  

^a NATIONAL ENVIRONMENTAL RESEARCH INSTITUTE   (Denmark)

^b NORWEGIAN POLAR INSTITUTE   (Norway)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^e NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^f ENVIRONMENT CANADA   (Canada)

^g UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Arctic fox; Embryonal ducts; Endocrine disruptors; Histopathology; Hyperplasia; OCs; Organochlorines; PCB; Thyroid; Thyroid C cell hyperplasia; Thyroid cysts; Ultimobranchial ducts

Indexed keywords

CARBENDAZIM; CHLORPHENOTANE; LINDANE; MUCIN; ORGANOCHLORINE DERIVATIVE; POLYCHLORINATED BIPHENYL;

ARCTIC ENVIRONMENT; CANID; CONCENTRATION (COMPOSITION); ENDOCRINE DISRUPTOR; HISTOPATHOLOGY; ORGANOCHLORINE; PCB;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL FOOD; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM METABOLISM; CONTROLLED STUDY; DIETARY INTAKE; ENDOCRINE DISEASE; ENERGY METABOLISM; ENVIRONMENTAL EXPOSURE; FOOD COMPOSITION; FOX; HISTOPATHOLOGY; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNE DEFICIENCY; INFLAMMATORY CELL; LEUKOCYTE; MALE; NONHUMAN; PORK; PREVALENCE; PRIORITY JOURNAL; SQUAMOUS EPITHELIUM; THYROID CELL; THYROID CYST; THYROID DISEASE; THYROID HYPERPLASIA; VULPES LAGOPUS;

ADIPOSE TISSUE; ANIMALS; DIET; DIETARY FATS; ENDOCRINE DISRUPTORS; ENERGY METABOLISM; ENVIRONMENTAL POLLUTANTS; FOOD CHAIN; FOXES; HYDROCARBONS, CHLORINATED; MALE; THYROID GLAND; TIME FACTORS;

ALOPEX LAGOPUS; ANIMALIA; BALAENOPTERA ACUTOROSTRATA; CANIDAE; SUS SCROFA; VULPES LAGOPUS;

EID: 67649601523     PISSN: 00139351     EISSN: 10960953     Source Type: Journal    
DOI: 10.1016/j.envres.2009.04.008     Document Type: Article

References (70)

1. AMAP, 1998. Persistent organic pollutants. AMAP assessment 1998. Arctic Monitoring and Assessment Programme, Oslo, pp. 183-372.
2. AMAP, 2004. AMAP Assessment 2002: persistent organic pollutants in the arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo, Norway, 310pp.
3. Baccarelli A., Giacomini S.M., Corbetta C., Landi M.T., Bonzini M., Consonni D., Grillo P., Patterson D.G., Pesatori A.C., and Bertazzi P.A. Neonatal thyroid function in seveso 25 years after maternal exposure to dioxin. PLoS Med. 5 (2008) 1133-1142
4. Bancroft J.D., and Stevens A. Theory and Practice of Histological Techniques (1996), Churchill Livingstone, New York pp. 186-187
5. Braathen M., Derocher A.E., Wiig Ø., Sørmo E.G., Lie E., Skaare J.U., and Jenssen B.M. Relationships between PCBs and thyroid hormones and retinol in female and male polar bears. Environ. Health Perspect. 112 (2004) 826-833
6. Brandt I., Jönsson C.J., and Lund B.O. Comparative studies on adrenocorticolytic DDT-metabolites. Ambio 21 (1992) 602-605
7. Brouwer A., Morse D.C., Lans M.C., Schuur G., Murk A.J., Klasson-Wehler E., Bergman A., and Visser T.J. Interactions of persistent environmental organohalogens and the thyroid hormone system: mechanisms and possible consequences for animal and human health. Toxicol. Ind. Health 14 (1998) 59-84
8. Capen, C.C., 2007. The endocrine glands. In: Jubb, K.V.F., Kennedy, P.C., Palmer, N. (Eds.), Pathology of Domestic Animals, fifth ed., vol. 3. Academic Press, San Diego, 771pp.
9. Colborn T., and Clement C. Chemically-Induced Alterations in Sexual and Functional Development: the Wildlife/Human Connection (1992), Princeton Scientific Pub. Co., Princeton, NJ, USA 403pp.
10. Colborn T. Neurodevelopment and endocrine disruption. Environ. Health Perspect. 112 (2004) 944-949
11. Colborn T., Saal F.S.V., and Soto A.M. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health Perspect. 101 (1993) 378-384
12. Conde E., Martin-Lacave I., Utrilla J.C., Moreno A., Gonzalez-Campora R., and Galera-Davidson H. Mitotic activity of the endocrine cells in rat thyroid glands during postnatal life. Endocrinology 131 (1992) 436-440
13. Darnerud P.O., and Sinjari T. Effects of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) on thyroxine and TSH blood levels in rats and mice. Organohalogen Compds. 29 (1996) 316-319
14. Das K., Vossen A., Tolley K., Vikingsson G., Thron K., Muller G., Baumgartner W., and Siebert U. Interfollicular fibrosis in the thyroid of the harbour porpoise: an endocrine disruption?. Arch. Environ. Contam. Toxicol. 51 (2006) 720-729
15. Fadden, M.F.K., 1994. Domestic dogs (Canis familiaris) as sentinels of environmental health hazards: the use of canine bioassays to determine alterrations in immune system. PhD Thesis, Cornell University, USA. UMI Dissertation Information Service, University Microfilms International, A Bell & Howell Information Company, Ann Arbor, Michigan 48106.
16. Faroon O.N., Jones D., and de Rosa C. Effects of polychlorinated biphenyls on the nervous system. Toxicol. Ind. Health 16 (2001) 305-333 (Review)
17. Foley D.S., and Fallat M.E. Thyroglossal duct and other congenital midline cervical anomalies. Sem. Pediatr. Surg. 15 (2006) 70-75
18. Ganong W.F. Review of Medical Physiology. 22nd ed. (2005), Appleton and Lange, USA 928pp.
19. Grandjean P., and Landrigan P.J. Review: developmental neurotoxicity of industrial chemicals. Lancet 16 (2006) 2167-2178
20. Grandjean P., Weihe P., Burse V.W., Needham L.L., Storr-Hansen E., Heinzow B., Debes F., Murata K., Simonsen H., Ellefsen P., Budtz-Jørgensen E., Keiding N., and White R.F. Neurobehavioral deficits associated with PCB in 7-year-old children prenatally exposed to seafood neurotoxicants. Neurotoxicol. Teratol. 23 (2001) 305-317
21. Grandjean P., White R.F., Sullivan K., Debes F., Murata K., Otto D.A., and Weihe P. Impact of contrast sensitivity performance on visually presented neurobehavioral tests in mercury-exposed children. Neurotoxicol. Teratol. 23 (2001) 141-146
22. Hallanger, I.G., 2005. Vitamin and hormone status in PCB exposed juvenile male (Alopex lagopus). Master Thesis in Physiology, Department of Biology, NTNU, Trondheim, Norway.
23. Heaton S.N., Bursian S.J., Giesy J.P., Tillitt D.E., Render J.A., Jones P.D., Verbrugge D.A., Kubiak T.J., and Aulerich R.J. 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 (1995) 334-343
24. Hertz-Picciotto I., Park H.Y., Dostal M., Kocan A., Trnovec T., and Sram R. Prenatal exposures to persistent and non-persistent organic compounds and effects on immune system development. Basic Clin. Pharmacol. Toxicol. 102 (2008) 146-154
25. Hobbs K.E., Muir D.C., Michaud R., Béland P., Letcher R.J., and Nortrom R.J. PCBs and organochlorine pesticides in blubber biopsies from free-ranging St. Lawrence River estuary beluga whales (Delphinapterus leucas), 1994-1998. Environ. Pollut. 122 (2003) 291-302
26. Jacobson J.L., and Jacobson S.W. Intellectual impairment in children exposed to polychlorinated biphenyls in utero. N. Engl. J. Med. 335 (1996) 783-789
27. Jenssen B.M. Endocrine-disrupting chemicals and climate change: a worst-case combination for Arctic marine mammals and seabirds?. Environ. Health Perspect. 114 (2006) 76-80
28. Johansen, P., Muir, D.C.G., Asmund, G., Rigét, F.F., 2004. Contaminants in traditional Greenland diet. Report to the Denmark Department of Environment, National Environmental Research Institute, Roskilde DK. NERI Technical Report, No. 492, 77pp.
29. Jönsson C.J., Lund B.O., and Brandt I. Adrenocorticolytic DDT metabolites: studies in mink, Mustela vison and otter, Lutra lutra. Ecotoxicology 2 (1993) 41-53
30. Kameda T. Immunohistochemical demonstration of keratins in the cysts of thyroid glands, parathyroid glands, and c-cell complexes of the dog. Am. J. Anat. 180 (1987) 87-99
31. Kilic N., Sandal S., Colakoglu N., Kutlu S., Seyran A., and Yilmaz B. Endocrine disruptive effects of polychlorinated biphenyls on the thyroid gland in female rats. Tohoku J. Exp. Med. 206 (2005) 327-332
32. Klaassen C.D., Amdur M.O., and Doull J. Casarett and Doulls Toxicology. The Basic Science of Poisons (2006), McGraw-Hill, New York 1111pp
33. Klecha A.J., Barreiro Arcos M.L., Frick L., Genaro A.M., and Cremaschi G. Immune-endocrine interactions in autoimmune thyroid diseases. Neuroimmunomodulation 15 (2008) 68-75
34. Köhrle J. Environment and endocrinology: the case of thyroidology. Ann. Endocrinol. (Paris) 69 (2008) 116-122
35. Langer P. Persistent organochlorinated pollutants (PCB, DDE, HCB, dioxins, furans) and the thyroid-review 2008. Endocr. Regul. 42 (2008) 79-104
36. Lans M.C., Klasson-Wehler E., Willemsen M., Meussen E., Safe S., and Brouwer A. Structure-dependent, competitive interaction of hydroxy-polychlorobiphenyls, hydroxy-dibenzo-pdioxins and hydroxy-dibenzofurans with human transthyretin. Chem.-Biol. Interact. 88 (1993) 7-21
37. Lans M.C., Spiertz C., Brouwer A., and Koeman J.H. Different competition of thyroxine binding to transthyretin and thyroxine binding globulin by hydroxy-polychlorobiphenyls, -dibenzo-p-dioxins and -dibenzofurans. Eur. J. Pharm.-Environ. 270 (1994) 129-136
38. Larsen, H.J.S., Sonne, C., Dietz, R., Kirkegaard, M., Letcher, R.J., 2009. The effect of high POP exposure on neonatal specific antibody formation in sledge dogs. J. Toxicol. Environ. Health A, to be submitted.
39. Letcher R.J., Klasson-Wehler E., and Bergman A. Methyl sulfone and hydroxylated metabolites of polychlorinated biphenyls. In: Paasivirta J. (Ed). The Handbook of Environmental Chemistry. Part K, New Types of Persistent Halogenated Compounds vol. 3 (2000), Springer, Berlin, Heidelberg, Germany 315-360
40. Lie E., Larsen H.J.S., Larsen S., Johansen G.M., Derocher A.E., Lunn N.J., Norstrom R.J., Wiig Ø., and Skaare J.U. Does high organochlorine (OC) exposure impair the resistance to infection in polar bears (Ursus maritimus)? Part I: Effect of OCs on the humoral immunity?. J. Toxicol. Environ. Health A 67 (2004) 555-582
41. Lie E., Larsen H.J.S., Larsen S., Johansen G.M., Derocher A.E., Lunn N.J., Norstrom R.J., Wiig Ø., and Skaare J.U. Does high organochlorine (OC) exposure impair the resistance to infection in polar bears (Ursus maritimus)? Part II: Possible effects of OCs on mitogen- and antigen-induced lymphocyte proliferation. J. Toxicol. Environ. Health A 68 (2005) 457-484
42. Lund B.O., Örberg J., Bergman A., Larsson C., Bergman A., Bäcklin B.M., Håkansson H., Madej A., Brouwer A., and Brunström B. Chronic and reproductive toxicity of a mixture of 15 methylsulfonyl-polychlorinated biphenyls and 3-methylsulvonyl-2,2-bis-(4-chlorophenyl)-1,1-dichlorethene in mink (Mustela vison). Environ. Toxicol. Chem. 18 (1999) 292-298
43. Lyon H., Andersen A.P., Hasselager E., Høyer P.E., Møller M., Prentø P., and Van Deurs B. Theory and Strategy in Histochemistry (1991), Springer, Berlin, Germany
44. Maervoet J., Vermeir G., Covaci A., Van Larebeke N., Koppen G., Schoeters G., Nelen V., Baeyens W., Schepens P., and Viaene M.K. Association of thyroid hormone concentrations with levels of organochlorine compounds in cord blood of neonates. Environ. Health Perspect. 115 (2007) 1780-1786
45. Martin P.A., Mayne G.J., Bursian S., Palace V., and Kannan K. Changes in thyroid and vitamin A status in mink fed polyhalogenated-aromatic-hydrocarbon-contaminated carp from the Saginaw River, Michigan, USA. Environ. Res. 101 (2006) 53-67
46. Meijer L., Weiss J., Van Velzen M., Brouwer A., Bergman A., and Sauerf P.J.J. Serum concentrations of neutral and phenolic organohalogens in pregnant women and some of their infants in the Netherlands. Environ. Sci. Technol. 42 (2008) 3428-3433
47. Mikaelian I., Labelle P., Kopal M., De Guise S., and Martineau D. Adenomatous hyperplasia of the thyroid gland in beluga whales (Delphinapterus leucas) from the St. Lawrence estuary and Hudson Bay, Quebec, Canada. Vet. Pathol. 40 (2003) 698-703
48. Morse D.C., Groen D., Veerman M., Van Amerongen C.J., Koeter H.B.W.M., Smits Van Prooije A.E., Visser T.J., Koeman J.H., and Brouwer A. Interference of polychlorinated biphenyls in hepatic and brain thyroid hormone metabolism in fetal and neonatal rats. Toxicol. Appl. Pharmacol. 122 (1993) 27-33
49. Morse, D.C., 1995. Polychlorinated biphenyl-induced alterations of thyroid hormone homeostasis and brain development in the rat. Ph.D. Thesis, Department of Toxicology, Agricultural University, Wageningen, The Netherlands.
50. Nieminen P., Hyvärinen H., Käkelä R., and Asikainen J. Plasma leptin and thyroxine of mink (Mustela vison) vary with gender, diet and subchronic exposure to PCBs. Comp. Biochem. Physiol. 127A (2000) 515-522
51. Otake T., Yoshinaga J., Enomoto T., Matsuda M., Wakimoto T., Ikegami M., Suzuki E., Naruse H., Yamanaka T., Shibuya N., Yasumizu T., and Kato N. Thyroid hormone status of newborns in relation to in utero exposure to PCBs and hydroxylated PCB metabolites. Environ. Res. 105 (2007) 240-246
52. Reid I.R. Anti-resorptive therapies for osteoporosis. Semin. Cell Dev. Biol. 19 (2008) 473-478
53. Rogstad, T.W., Jenssen, B.M., Villanger, G.D., Ahlstrøm, Ø., Fuglei, E., Muir, D., Sonne, C., Jørgensen, E., 2009. Exposure to high PCB diet reduces alpha-tochopherol levels and disrupts thyroid hormone balance in blue foxes (Alopex lagopus). Environ Research, to be submitted.
54. Sandau C.D., Ayotte P., Dewailly E., Duffe J., and Norstrom R.J. Pentachlorophenol and hydroxylated polychlorinated biphenyl metabolites in umbilical cord plasma of neonates from coastal populations in Quebec. Environ. Health Perspect. 110 (2002) 411-417
55. Sanders E.J., and Harvey S. Peptide hormones as developmental growth and differentiation factors. Dev. Dyn. 237 (2008) 1537-1552
56. Schell L.M., Gallo M.V., Denham M., Ravenscroft J., DeCaprio A.P., and Carpenter DO. Relationship of thyroid hormone levels to levels of polychlorinated biphenyls, lead, p,p′ -DDE, and other toxicants in Akwesasne Mohawk youth. Environ. Health Perspect. 116 (2008) 806-813
57. Schuur A.G., van Meeteren M.E., Jong W.M.C., Bergman A., Visser T.J., and Brouwer A. Polybrominated biphenyl and diphenylether flame retardants: analysis, toxicity and environmental occurrence. Organohalogen Compds. 28 (1996) 509-512
58. Schuur A.G., Legger F.F., van Meeteren M.E., Moonene M.J.H., van Leeuwen-Bol I., Bergman A., and Visser T.J. In vitro inhibition of thyroid hormone sulfation by hydroxylated metabolites of halogenated aromatic hydrocarbons. Chem. Res. Toxicol. 11 (1998) 1075-1081
59. Schuur A.G., Bergman A., Brouwer A., and Visser T.J. Effects of pentachlorophenol and hydroxylated polychlorinated biphenyls on thyroid hormone conjugation in a rat and a human hepatoma cell line. Toxicol. In Vitro 13 (1999) 417-425
60. Sinjari T., and Darnerud P.O. Hydroxylated polychlorinated biphenyls: placental transfer and effects on thyroxine in the foetal mouse. Xenobiotica 28 (1998) 21-30
61. Skaare J.U., Bernhoft A., Wiig Ø., Norum K.R., Haug E., Eide D.M., and Derocher A.M. Relationship between plasma levels of organochlorines, retinol and thyroid hormones from polar bears (Ursus maritimus) at Svalbard. J. Toxicol. Environ. Health A 62 (2001) 227-241
62. Solomon J.R., and Rangecroft L. Thyroglossal duct lesions in childhood. J. Pediatr. Surg. 19 (1984) 555-558
63. Sonne C., Dietz R., Larsen H.J.S., Loft K.E., Kirkegaard M., Letcher R.J., Shahmiri S., and Møller P. Impairment of cellular immunity in West Greenland sledge dogs (Canis familiaris) dietary exposed to polluted Minke Whale (Balaenoptera acutorostrata) Blubber. Environ. Sci. Technol. 40 (2006) 2056-2062
64. Sonne C., Fonfara S., Dietz R., Kirkegaard M., Letcher R.J., Shahmiri S., Andersen S., and Møller P. Multiple cytokine and acute phase protein gene transcription in West Greenland sledge dogs (Canis familiaris) dietary exposed to organic environmental pollutants. Arch. Environ. Contam. Toxicol. 53 (2007) 110-118
65. Sonne C., Leifsson P.S., Wolkers H., Jenssen B.M., Fuglei E., Ahlstrøm Ø., Dietz R., Kirkegaard M., Muir D.C.G., and Jørgensen E. Organochlorine-induced histopathology in kidney and liver tissue from Arctic fox (Alopex lagopus). Chemosphere 71 (2008) 1214-1224
66. Sonne C., Wolkers H., Rigét F.F., Beck Jensen J.E., Teilmann J., Jenssen B.M., Fuglei E., Ahlstrøm Ø., Dietz R., Muir D.C.G., and Jørgensen E. Mineral density and biomechanical properties of bone tissue from male Arctic foxes (Vulpes lagopus) exposed to organochlorines and emaciation. Comp. Biochem. Phys. C 149 (2008) 97-103
67. Tauson A.H., Chwalibog A., and Ahlstrøm Ø. Substrate oxidation in male blue foxes (Vulpes lagopus) during feeding, fasting realimentation. J. Nutr. 132 (2002) 1793S-1795S
68. Telander R.L., and Deane S.A. Thyroglossal and branchial cleft systs and sinuses. Surg. Clin. North Am. 57 (1977) 779-791
69. Wang S.L., Su P.H., Jong S.B., Guo Y.L., Chou W.L., and Papke O. In utero exposure to dioxins and polychlorinated biphenyls and its relations to thyroid function and growth hormone in newborns. Environ. Health Perspect. 113 (2005) 1645-1650
70. Williams E.D., Toyn C.E., and Harach H.R. The ultimobranchial gland and congenital thyroid abnormalities in man. J. Pathol. 159 (1989) 135