[en] The thyroid plays an important role in development and is of primary importance in metabolism and heat loss for cetaceans, including the harbor porpoise (Phocoena phocoena). Several studies have demonstrated that environmental contaminants can alter various aspects of thyroid function in mammals and may contribute to various histologic changes. The present study completes the data set of a 2006 study by Das et al., by performing histological and immunohistologic investigations on thyroids of 36 harbor porpoises from Belgian and United Kingdom waters. The number and mean diameter of follicles (µm) and the relative proportion of follicular, connective, and vascular tissue (%) were quantified in the thyroid gland of each individual. Interfollicular fibrosis has been observed in these thyroid glands, and the collective findings support the hypothesis of an endocrine disruption of thyroid function through organochlorinated compounds. Our study aimed also to reveal potential relationships between thyroid morphometric data and metal levels (Cd, Fe, Zn, Cu, Se, and Hg) using multivariate statistical analysis. The multiple regressions revealed statistically significant relationships between trace elements (cadmium, selenium, and copper) and thyroid fibrosis. The largely negative relationships are interesting findings but do not support the hypothesis that these elements have an adverse effect on thyroid morphometry. Further research is needed to understand the nature of any relationship between organochlorine and trace element exposure and thyroid gland morphology and function in harbor porpoises.
Disciplines :
Sciences aquatiques & océanologie
Auteur, co-auteur :
Schnitzler, Joseph ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Siebert, Ursula; Research- and Technology Centre Westcoast > Christian-Albrecht-University Kiel > Büsum, Germany
Jepson, Paul; Institute of Zoology > Zoological Society of London > Regent’s Park, London NW1 4RY United Kingdom.
Beineke, Andreas; Institute of Pathology > University of Veterinary Medicine > Bünteweg 17, 30559 Hannover, Germany
Jauniaux, Thierry ; Université de Liège - ULiège > Département de morphologie et pathologie > Département de morphologie et pathologie
Bouquegneau, Jean-Marie ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Das, Krishna ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Langue du document :
Anglais
Titre :
Harbour porpoise thyroids: Histological investigations and potential interactions with environmental factors
ARTHUR, J. R., F. NICOL, E. GRANT, AND G. J. BECKETT. 1991. The effects of selenium deficiency on hepatic type-I iodothyronine deiodinase and protein disuphide-isomerase assessed by activity measurements and affinity labelling. Biochemical Journal 274: 297-300.
BAKER, V. A. 2001. Endocrine disrupters-testing strategies to assess human hazard. Toxicology in Vitro 15: 413-419.
BAUMCÄRTNER, W., C. ÖRVELL, AND M. REINACHER. 1989. Naturally occurring canine distemper virus encephalitis: Distribution and expression of viral polypeptides in nervous tissues. Acta Neuropathology 78: 504-512.
BEDWAL, R. S., AND A. BHUGUNA. 1994. Zinc, copper and selenium in reproduction. Experientia 50: 626-640.
BENKE, H., U. SIEBERT, R. LICK, B. BANDOMIR, AND R. WEISS. 1998. The current status of harbour porpoises (Phocoena phocoena) in German waters. Archives of Fishery and Marine Research 46: 97-123.
BENNETT, P. M., P. D. JEPSON, R. J. LAW, B. R. JONES, T. KUIKEN, J. R. BAKER, E. ROGAN, AND J. K. KIRKWOOD. 2001. Exposure to heavy metals and infectious disease mortality in harbour porpoises from England and Wales. Environmental Pollution 112: 33-40.
BLOOM, W., AND D. W. FAWCETT. 1975. The thyroid gland. In A textbook of histology. Saunders, Philadelphia, Pennsylvania. pp. 524-534.
BROUWER, A., P. J. H. REIJNDERS, AND J. H. KOEMAN. 1989. Polychlorinated biphenyl (PCB)-contaminated fish induces vitamin A and thyroid hormone deficiency in the common seal (Phoca vitulina). Aquatic Toxicology 15: 99-105.
BROUWER, A., M. P. LONGNECKER, L. S. BIRNBAUM, J. COGLIANO, P. KOSTYNIAK, J. MOORE, S. SCHANTZ, AND G. WINNEKE. 1999. Characterization of potential endocrine related health effects at low-dose levels of exposure to PCB's. Environmental Health Perspectives 107: 639-649.
BYRNE, J. J., J. P. CARBONE, AND E. A. HANSON. 1987. Hypothyroidism and abnormalities in the kinetics of thyroid hormone metabolism in rats treated chronically with polychlorinated biphenyl and polybrominated biphenyl. Endocrinology 121: 520-527.
COVACI, A., K. I. VAN DE VIJVER, W. M. DE COEN, K. DAS, J. M. BOUQUEGNEAU, R. BLUST, AND P. SCHEPENS. 2002. Determination of organohalogenated contaminants in liver of harbour porpoises ( Phocoena phocoena) stranded on the Belgian North Sea coast. Marine Pollution Bulletin 44: 1152-1169.
COWAN, D. F., AND Y. TAJIMA. 2006. The thyroid gland in bottlenose dolphins (Tursiops truncatus) from the Texas coast of the Gulf of Mexico: Normal structure and pathological changes. Journal of Comparative Pathology 135: 217-225.
DAMSTRA, T., S. BARLOW, A. BERGMAN, R. KAVLOCK, AND G. VAN DER KRAAK. 2002. General conclusions and research needs. In Global assessment of the state-of-science of endocrine disruptors, T. Damstra, S. Barlow, A. Bergman, R. Kavlock and G. Van Der Kraak (eds.). World Health Organization, Geneva, Switzerland, pp. 130-133.
DAS, K., V. DEBACKER, AND J. M. BOUQUEGNEAU. 2000. Metallothioneins in marine mammals. Cellular and Molecular Biology 46: 283-294.
DAS, K., C. BEANS, L. HOLSBEEK, G. MAUGER, S. D. BERROW, E. ROGAN, AND J. M. BOUQUFGNEAU. 2003. Marine mammals from northeast Atlantic: Relationship between their trophic status as determined by [delta]13C and [delta]15N measurements and their trace metal concentrations. Marine Environmental Research 56: 349-365.
DAS, K., U. SIEBERT, M. FONTAINE, T. JAUNIAUX, L. HOLSBEEK, AND J.-M. BOUQUEGNEAU. 2004. Ecological and pathological factors related to trace metal concentrations in harbour porpoises from the North Sea and adjacent areas. Marine Ecology Progress Series 281: 283-295.
DAS, K., A. DEGROOF, T. JAUNIAUX, AND J. M. BOUQUEGNEAU. 2006a. Zn, Cu, Cd and Hg binding to metallothioneins in harbour porpoises Phocoena phocoena from the southern North Sea. BMC Ecology 6.2, doi 10.1186/1472-6785-6-2.
DAS, K., A. VOSSEN, K. TOLLEY, G. VIKINGSSON, K. THRON, G. MÜLLER, W. BAUMCARTNER, AND U. SIEBERT. 2006b. Interfollicular fibrosis in the thyroid of the harbour porpoise: An endocrine disruption? Archives of Environmental Contamination and Toxicology 51: 720-729.
DEBIER, C., G. M. YLITALO, M. WEISE, F. GULLAND, D. P. COSTA, B. J. LE BOEUF, T. DE TILLESSE, AND Y. LARONDELLE. 2005. PCBs and DDT in the serum of juvenile California sea lions: Associations with vitamin A and E and thyroid hormones. Environmental Pollution 134: 323-332.
DE GUISE, S., D. MARTINEAU, P. BÉLAND, AND M. FOURNIER. 1995. Possible mechanisms of action of environmental contaminants on St. Lawrence beluga whales (Delphimapterus leucas). Environmental Health Perspectives 103: 73-77.
ESIPENKO, B. E., AND N. V. MARSAKOVA. 1990. The effect of copper on the metabolism of iodine, carbohydrates and proteins in rats. Fiziologicheskiǐ Zhurnal 36: 35-43.
FELDMAN, E. C., AND R. W. NELSON. 1998. Hypothyroidism. In Canine and feline endocrinology and reproduction. W. B. Saunders Company, St. Louis, Missouri. pp. 68-117.
GELBKE, H. P., M. KAYSER, AND A. POOLE. 2004. OECD test strategies and methods for endocrine disruptors. Toxicology 205: 17-25.
GROSH, N., AND A. S. BHATTACHARY. 1992. Thyrotoxicity of the chlorides of cadmium and mercury in rabbit. Biomedical and Environmental Science 5: 236A-240A.
GOEL, A., D. DHAWAN, AND S. KHERUKA. 1994. Evaluation of zinc in the regulation of serum T3 and T4 levels and hepatic functions in carbontetrachloride-intoxicated rats. Biological Trace Element Research 41: 58-68.
GREGORY, M., AND D. G. CYR. 2003. Effects of environmental contaminants on the endocrine system of marine mammals. In Toxicology of Marine Mammals, J. G. Vos, G. Bossart, M. Fournier, and T. O'Shea (eds.). Taylor and Francis, Washington, DC, pp. 67-81.
GUPTA, P., AND A. KAR. 1998. Role of ascorbic acid in cadmium-induced thyroid dysfunction and lipid peroxidation. Journal of Applied Toxicology 18: 317-320.
GUPTA, P., AND A. KAR 1999. Cadmium induced thyroid dysfunction in chickens: Hepatic type I iodothyronine 5′-monodeiodinase activity and role of lipid peroxidation. Comparative Biochemistry and Physiology 123: 39-44.
GUPTA, S. S. CHAURASIA, P. K. MAITI, AND A. KAR. 1997a. Cadmium induced alteration in extra-thyroidal conversion of thyroxine to trithyronine by type-I iodothyronine 5′-monodeiodinase in male mouse. Hormone and Metabolic Research 29: 155-156.
GUPTA, P. C. VERMA, AND S. L. GARG. 1997b. Effect of experimental zinc deficiency on thyroid gland in guinea pigs. Annals of Nutrition and Metabolism 41: 376-381.
HALL, A. J., O. I. KALANTZI, AND G. O. THOMAS. 2003. Polybromonated diphenyl ethers (PBDEs) in grey seals during their first year of life-are they thyroid hormone endocrine disrupters? Environmental Pollution 126: 29-37.
HALLGREN, S., AND P. O. DARNERUD. 2002. Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and chlorinated paraffins (CPs) in rats-testing interactions and mechanisms for thyroid hormone effects. Toxicology 177: 227-243.
HOWDESHELL, K. L. 2002. A model of the development of the brain as a construct of the thyroid system. Environmental Health Perspectives 110: 337-348.
HUTCHINSON, T. H., R. BROWN, K. E. BRUGGER, P. M. CAMPELL, M. HOLT, R. LÄNGE, P. MCCAHON, L. J. TATTERSFIELD, AND R. VAN EGMOND. 2000. Ecologićal risk assessment of endocrine disruptors. Environmental Health Perspectives 108: 1007-1014.
ISHIHARA, A., S. SAWATSUBASHI, AND K. YAMAUGHI. 2003. Endocrine disrupting chemicals: Interference of thyroid hormone binding to transthyretins and to thyroid hormone receptors. Molecular and Cellular Endocrinology 199: 105-117.
JEPSON, P. D. 2003. Pathology and toxicology of stranded harbour porpoises (Phocoena phocoena) in UK waters. Royal Veterinary College University, London, UK.
JUBB, K. V. F., P. C. KENNEDY, AND N. PALMER. 1993. Thyroid gland. In Pathology of domestic animals. Academic Press, San Diego, California. pp. 306-329.
JUNQUEIRA, L. C., J. CARNEIRO, AND R. O. KELLEY. 1995. Thyroid gland. In Basic histology, J. Dolan and C. Langan (eds.). The McGraw-Hill Companies, Rio de Janeiro, Brazil. pp. 398-406.
KAWADA, J., M. NISHIDA, Y. YOSHIMARA, AND K. MITANI. 1980. Effects of organic and inorganic mercurial on thyroidal functions. Journal of Pharmacobio-dynamics 3: 149-159.
KEITH, L. H. 1997. Environmental endocrine disruptors: A handbook of proprieties. John Wiley and Sons, New York, New York, 1,232 pp.
KRALIK, A., M. KIRCHGESSNER, AND K. EDER. 1996. Concentration of thyroid hormones in serum and activity of hepatic 5′ monodeiodinase in copper deficient rats. Zeitschriff für Ernäbrungwissenschaft 35: 288-291.
LAW, R. J. 1994. Collaborative UK marine mammal project: Summary of data produced 1988-1992. Fisheries Research Technical Report 97. Directorate of Fisheries Research, Ministry of Agriculture, Fisheries and Food, Lowestoft, UK.
LOCKYER, C. 1995. A review of factors involved in zonation in Odontocetes teeth, and an investigation of the likely impact of environmental factors and major life events on harbour porpoise tooth structure. In Biology of phocoenids: International Whaling Commission, A. Bjorge and J. P. Donovan (eds.). International Whaling Commission Cambridge, pp. 511-529.
NISHIDA, M., T. YAMAMOTOET, Y. YOSHIMARA, AND J. KAWADA. 1986. Subacute toxicity of methylmercuric chloride and mercuric chloride on mouse thyroid. Journal of Pharmacobio-dynamics 9: 331-338.
NISHIJO, M., H. NAKAGAWA, Y. MORIKAWA, M. TABATA, M. SENMA, K. MIURA, I. TSURITANI, R. HONDA, T. KIDO, AND H. TERANISHI, ET AL. 1994. A study of thyroid hormone levels of inhabitants of the cadmium polluted Kakehashi River basin. Nippon Eiseigaku Zasshi 49: 598-609. [IN JAPANESE]
OLIVER, J. W. 1975. Interrrelationships between athyroetic and copper-deficient states in rats. American Journal of Veterinary Research 36: 1649-1653.
PAVIA J'UNIOR, M. A., B. PAIER, M. I. NOLI, K. HAGMÜLLER, AND A. A. ZANINOVICH. 1997. Evidence suggesting that cadmium induces a nonthyroidal illness syndrome in the rat. Journal of Endocrinology 154: 113-117.
REIJNDERS, P. J. H. 1994. Toxicokinetics of chlorobiphenyls and associated physiological responses in marine mammals, with particular reference to their potential for ecotoxicological risk assessment. Science of the Total Environment 154: 229-236.
RICHARD, P. R., A. R. MARTIN, AND J. R. ORR. 2001. Summer and autumn movements of belugas of the Eastern Beaufort Sea stock. Arctic 54: 223-236.
ROLLAND, R. M. 2000. A review of chemically-induced alterations in thyroid and vitamin A status from field studies of wildlife and fish. Journal of Wildlife Diseases 36: 615-635.
ROSA, C., O'HARA, T. M., P. F. HOEKSTRA, K. R. REFSAL, AND J. E. BLAKE. 2007. Serum thyroid hormone concentrations and thyroid histomorphology as biomarkers in bowhead whales (Balaena mysticetus). Canadian Journal of Zoology-Revue Canadienne de Zoologie 85: 609-618.
RUZ, M., J. CODOCEO, J. GALGANI, L. MUNOZ, N. GRAS, S. MUZZO, L. LEIVA, AND C. BOSCO. 1999. Single and multiple selenium-zinc-iodine deficiencies affect rat thyroid metabolism and ultrastructure. Journal of Nutrition 129: 174-180.
SCHNITZLER, J. G. 2005. Etude histomorphométrique de la glande thyroïde do marsouin common (Phocoena phocoena) (L.): Relation potentielle avec différents organohalogénés. Dissertation. Université de Liège, Liège, France.
SCHUMACHER, U., S. ZAHLER, H.-P. HORNY, G. HEIDEMANN, K. SKIRNISSON, AND U. WELSCH. 1993. Histological investigations on the thyroid gland of marine mammals (Phoca vitulina, Phocoena phocoena) and the possible implication of marine pollution. Journal of Wildlife Diseases 29: 103-108.
SHIMOKAWA, T., I. NAKANISHI, E. HONDO, T. IWASAKI, Y. KISO, AND T. MAKITA. 2002. A morphological study of the thyroid gland in Risso's dolphin, Grampus griseus. Journal of Veterinary Medical Science 64: 509-512.
SIEBERT, U., C. JOIRIS, L. HOLSBEEK, H. BENKE, K. FAILING, K. FRESE, AND E. PETZINGER. 1999. Potential relation between mercury concentrations and necropsy findings in cetaceans from German waters of the North and Baltic Seas. Marine Pollution Bulletin 38: 285-329.
SIEBERT, U., C. JOIRIS, A. VOSSEN, W. BAUMGARTNER, G. MULLER, A. BEINEKE, M. MCLACHAN, R. BRUHN, AND K. THRON. 2002. Untersuchungen zu Auswirkungen von Umweltchemikalien auf das Endokrinium und Immunsystem von Schweinswalen aus der deutschen Nord- und Ostsee. FTZ, Kiel, Germany, 303 pp.
SKAARE, J. U., H. J. LARSEN, E. LIE, A. BERNHOFT, A. E. DEROCHER, R. NORSTROM, E. ROPSTAD, N. F. LUNN, AND O. WIIG. 2002. Ecological risk assessment of persistent organic pollutants in the arctic. Toxicology 181: 193-197.
SLIJPER, E. J. 1973. Die Organe des Halses und des vorderen Thoraxabschnittes. In Die Cetaceen. A. Asher and Co., Amsterdam, The Netherlands. pp. 137-140.
ST AUBIN, D. J., AND J. R. GERACI. 1989. Adaptive-changes in hematologic and plasma chemical-constituents in captive beluga whales, Delphinapterus-Leucas. Canadian Journal of Fisheries and Aquatic Sciences 46: 796-803.
ST AUBIN, D. J., S. H. RIDGWAY, R. S. WELLS, AND H. RHINEHART. 1996. Dolphin thyroid and adrenal hormones: Circulating levels in wild and semi-domesticated Tursiops truncatus, and influence of sex, age, and season. Marine Mammal Science 12: 1-13.
TSOU, C. T., M. D. CHEN, W. H. LIN, AND L. T. HO. 1993. Alterations of zinc levels in patients with thyroid disorders. Chung Hua I Hsueh Tsa Chih 51: 57-60.
WOLDSTAD, S., AND B. M. JENSSEN. 1999. Thyroid hormones in grey seal pups (Halichoerus grypus). Comparative Biochemistry and Physiology Part A 122: 157-162.
WORTHY, G. A. J., AND E. F. EDWARDS. 1990. Morphometric and biochemical factors affecting heat loss in a small temperate cetacean (Phocoena phocoena) and a small tropical cetacean (Stenella attenuata). Physiological Zoology 63: 432-442.
WU, H. Y., Y. M. XIA, AND X. S. CHEN. 1995. Selenium deficiency and thyroid hormone metabolism and function. Sheng Li Ko Hsueh Chin Chan 26: 12-16.
ZHOU, T., H. B. JOHN-ALDEB, J. S. WEIS, AND P. WEIS. 2000. Endocrine disruption: Thyroid dysfunction in mummichogs (Fundulus heteroclitus) from a polluted habitat. Marine Environmental Research 50: 393-397.
ZIMMERMANN, M., P. ADOU, T. TORRESANI, C. ZEDER, AND R. HUBBELL. 2000. Iron supplementation in goitrous, iron deficient children improves their response to oral iodized oil. European Journal of Endocrinology 142: 217-223.
