Effects of persistent organic pollutants on the thyroid function of the European sea bass (Dicentrarchus labrax) from the Aegean Sea, is it an endocrine disruption?
[en] We evaluated the alterations of organochlorinated compounds such as polychlorobiphenyls (PCB), dichloro-diphenyl-dichloroethylene (DDE) and dichloro-diphenyl-trichloroethane (DDT) on the thyroid in wild and cultured sea bass (Dicentrarchus labrax) at environmental concentrations. These compounds influence the endocrine system of many fish species and are qualified as endocrine disruptors. The thyroid seems to be a target organ. Two alteration endpoints: the thyroid histology and the muscular thyroid hormone concentrations, were used simultaneously.
High concentrations in PCBs and DDT were detected in muscles, supporting the idea that the Mediterranean fauna could be more polluted than the Atlantic fauna. The high abundance of DDE indicates a progressive degradation of remnant DDT load and the absence of new inputs in this area. Aquaculture sea bass shows a significant higher amount of pollutants on fresh weight basis (especially PCBs) in their muscles compared to the wild sea bass. Those differences may be related mainly to the contaminations of diet.
Thyroid parameters vary between wild and aquaculture sea bass, wild sea bass were characterized by higher follicle diameters, epithelial cell heights and muscular T4 concentrations. A significant relationship between persistent organic pollutants (muscular PCBs and DDT concentration) and the different thyroid parameters (diameters of follicles, epithelial cell heights and muscular T4 levels) could be observed, which support the hypothesis that these compounds have an adverse impact on thyroid morphometry and function.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Schnitzler, Joseph ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Koutrarkis, Emmanuil; Fisheries Research Institute > National Agricultural Research Foundation > 640 07 Nea Peramos, Kavala, Greece
Siebert, Ursula; Research- and Technology Centre Westcoast > Christian-Albrecht-University Kiel > Büsum, Germany.
Thomé, Jean-Pierre ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Ecologie animale et écotoxicologie
Das, Krishna ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Language :
English
Title :
Effects of persistent organic pollutants on the thyroid function of the European sea bass (Dicentrarchus labrax) from the Aegean Sea, is it an endocrine disruption?
Aguilar A., and Borrell A. DDT and PCB reduction in the western Mediterranean from 1987 to 2002, as shown by levels in sriped dolphins (Stenella coerueoalba). Marine Environmental Research 59 (2005) 391-404
Antunes P., and Gil O. PCB and DDT contamination in cultivated and wild sea bass from Ria de Aveiro, Portugal. Chemosphere 54 (2004) 1503-1507
Antunes P., Gil O., and Reis-Henriques M.A. Evidence for higher biomagnification factors of lower chlorinated PCBs in cultivated sea bass. Science of the Total Environment 377 (2007) 36-44
Blanton M.L., and Specker J.L. The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction. Critical Reviews in Toxicology 37 (2007) 97-115
Boas M., Feldt-Rasmussen U., Skakkebaek N.E., and Main K.M. Environmental chemicals and thyroid function. European Journal of Endocrinology 154 (2006) 599-611
Braathen M., Derocher A.E., Wiig O., Sormo E.G., Lie E., Skaare J.U., and Jenssen B.M. Relationships between PCB's and thyroid hormones and Retinol in female polar bears. Environmental Health Perspectives 112 (2004) 826-833
Brouwer A., Reijnders P.J.H., and Koeman J.H. Polychlorinated biphenyl (PCB)-contaminated fish induces vitamin A and thyroid hormone deficiency in the common seal (Phoca vitulina). Aquatic Toxicology 15 (1989) 99-105
Brown S.B., Adams B.A., Cyr D.G., and Eales J.G. Contaminant effects on the teleost fish thyroid. Environmental Toxicology and Chemistry 23 (2004) 1680-1701
Canli M., and Atli G. The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six Mediterranean fish species. Environmental Pollution 121 (2003) 129-136
Carubelli G., Fanelli R., Mariani G., Nichetti S., Crosa G., Calamari D., and Fattore E. PCB contamination in farmed and wild sea bass (Dicentrarchus labrax L.) from a coastal wetland area in central Italy. Chemosphere 68 (2007) 1630-1635
Collins W.T., and Capen C.C. Biliary excretion of125 I-Thyroxine and fine structural alterations in the thyroid of Gunn Rats fed polychlorinated biphenyls (PCB). Laboratory Investigation 43 (1980) 158-164
Collins W.T., and Capen C.C. Fine structural lesions and hormonal alterations in thyroid glands of perinatal Rats exposed in Utero and by Milk to Polychlorinated Biphenyls. American Association of Pathologists 99 (1980) 125-142
Damstra T., Barlow S., Bergman A., Kavlock R., and Van Der Kraak G. Global Assessment of the State-of-Science of Endocrine Disruptors (2002), International Programme on Chemical Safety
Das K., Vossen A., Tolley K., Vikingsson G., Thron K., Müller G., Baumgartner W., and Siebert U. Interfollicular fibrosis in the thyroid of the harbour porpoise: an endocrine disruption?. Archives of Environmental Contamination and Toxicology 51 (2006) 720-729
Dassenakis M. Environmental problems of Greece from a chemical point of view. Chemistry International 22 (2000) 1-7
de Boers J., and Pieters H. Dietary accumulation of polychlorinated biphenyls, chlorinated pesticides and mercury in cultivated eels, Anguilla anguilla. Aquaculture and Fisheries Management 22 (1991) 329-334
Debier C., Ylitalo G.M., Weise M., Gulland F., Costa D.P., Le Boeuf B.J., de Tillesse T., and Larondelle Y. PCBs and DDT in the serum oh juvenile California sea lions: associations with vitamins A and E and thyroid hormones. Environmental Pollution 134 (2005) 323-332
Fossi M.C., Marsili L., Lauriano G., Fotrtuna C., Canese S., Ancora S., Leonzio C., Romeo T., Merino R., Abad E., and Jiménez B. Assessment of toxicological status of a SW Mediterranean segment population of striped dolphin (Stenella coerulealba) using skin biopsy. Marine Environmental Research 58 (2004) 269-274
Fowles J.R., Fairbrother A., Trust K.A., and Kerkvliet N.I. Effects of aroclor 1254 on the thyroid gland, immune function, and hepatic cytochrome P450 activity in Mallards. Environmental Research 75 (1997) 119-129
Gauger K.J., Kato Y., Haraguchi K., Lehmler H.-J., Robertson L.W., Bansal R., and Zoeller R.T. Polybrominated Biphenyls (PCB's) exert thyroid hormone-like effects in the fetal Rat brain but do not bind to thyroid hormone receptors. Environmental Health Perspectives 112 (2004) 516-523
Golfinopoulus S.K., Nikolaou A.D., Kostopoulou M.N., Xilourgidis N.K., Vagi M.C., and Lekkas D.T. Organochlorine pesticides in the surface waters of Northern Greece. Chemosphere 50 (2003) 507-516
Hall A.J., Green N.J.L., Jones K.C., Pomeroy P.P., and Harwood J. Thyroid hormones as biomarkers in grey seals. Marine Pollution Bulletin 36 (1998) 424-428
Hallgren S., and Darnerud P.O. Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and chlorinated paraffins (CPs) in rats-testing interactions and mechanisms for thyroid hormone effects. Toxicology 177 (2002) 227-243
Herbert C.E., and Keenleyside K.A. To normalize or not to normalize? Far is the question. Environmental Toxicology and Chemistry 14 (1995) 801-807
Howdeshell K.L. A model of the development of the brain as a construct of the thyroid system. Environmental Health Perspectives 110 (2002) 337-348
Ishihara A., Sawatsubashi S., and Yamauchi K. Endocrine disrupting chemicals: interference of thyroid hormone binding to transthyretins and to thyroid hormone receptors. Molecular and Cellular Endocrinology 199 (2003) 105-117
Janz D.M. In: Ostrander G.K. (Ed). Endocrine System (2000), The Laboratory Fish, San Diego, CA
Jefferies D.J., and French M.C. Avian thyroid: effect of p′p -DDT on size and activity. Science 166 (1969) 1278-1280
Jenssen G., Tyrhaug I.B., Sormo E.G., and Andersen O.K. Effects of PBDE-47 on thyroid and steroid hormone status in juvenile turbot (Schophtalamus maximus). Organohalogen Compounds 66 (2004) 3078-3081
Kallianiotis, A., Koutrakis, E., Kokkinakis, A.K., 2000. Fisheries in the Kavala Prefecture. The current situation, tendencies and impacts on the prefecture's coastal areas. ÔÅRRA Coastal Zone Management Project: "Preparing an Integrated Management Plan for the Coastal Zone of the Kavala Prefecture". Development Agency of the Prefectural Administration of Kavala, pp. 1-31.
Kallianiotis A., Vidoris P., and Sylaios G. Fish species assemblages and geographical sub-areas in the North Aegean Sea, Greece. Fisheries Research 68 (2004) 171-187
Kilikidis S.D., Psomas J.E., Kamarianos A.P., and Panetsos A.G. Monitoring of DDT, PCBs, and other organochlorine compounds in marine organisms from the North Aegean Sea. Journal Bulletin of Environmental Contamination and Toxicology 26 (1981) 496-501
Kobuke L., Specker J.L., and Bern H.A. Thyroxine content of eggs and larvae of coho salmon, Oncorhynchus kisutch. Journal of Experimental Zoology 242 (1987) 89-94
Koutrakis E., Kokkinakis A.K., Eleftheriadis E.A., and Argyropoulou M.D. Seasonal changes in distribution and abundance of the fish fauna in the two estuarine systems of Strymonikos gulf (Macedonia, Greece). Belgian Journal of Zoology 130 (2000) 43-50
Leatherland J.F. Field observation on reproductive and developmental dysfunction in introduced and native salmonids from the Great Lakes. Histochemical Journal 19 (1993) 737-751
Leatherland J.F., and Sonstegard R.A. Lowering of serum thyroxine and triiodothyronine levels in yearling coho salmon by dietary mirex and PCBs. Journal of the Fisheries Research Board of Canada 35 (1978) 1285-1289
Leatherland J.F., and Sonstegard R.A. Effect of dietary polychloninated biphenyls (PCBs) or mirex in combination with food deprivation and testosterone administration on serum thyroid hormone concentration and bioaccumulation of organochlorines in rainbow trout, Salmo gairdneri. Journal of Fish Diseases 3 (1980) 115-124
Loizeau V., Abarnou A., Cugier P., Jaouen-Madoulet A., Le Guellec A.-M., and Ménesguen A. A model of PCB bioaccumulation in the seabass food web from the Seine Estuary (eastern English Channel). Marine Pollution Bulletin 43 (2001) 242-255
Marsili L., and Focardi S. Organochlorine levels in subcutaneous blubber biopsies of fin whales (Balaenoptera physalus) and striped dolphins (Stenella coeruleoalba) from the Mediterranean Sea. Environmental Pollution 91 (1996) 1-9
Naso B., Perrone D., Ferrante M.C., Bilacione M., and Lucisano A. Persistent organic pollutants in edible marine species from the Gulf of Naples, Southern Italy. Science of the Total Environment 343 (2005) 83-95
Parker S.J. Thyroid hormone levels in Larval and Juvenile Strped Bass Morone saxatilis: Response to Changes in Salinity and Temperature (1988), University of Rhode Island, Providence pp. 1-147
Pastor D., Boix J., Fernandez V., and Albaiges J. Bioaccumulation of organochlorinated contaminants in three estuarine fish species (Mullus barbatus, Mugil cephalus and Dicentrarcus labrax). Marine Pollution Bulletin 32 (1996) 257-262
Plate E.M., Adams B.A., Allison W.T., Martens G., Hawryshyn C.W., and Eales J.G. The effects of thyroxine or a GnRH analogue on thyroid hormone deiodination in the olfactory epithelium and retina of rainbow trout, Oncorhynchus mykiss, and sockeye salmon, Oncorhynchus nerka. General and Comparative Endocrinology 127 (2002) 59-65
Power D.M., Llewellyn L., Faustino M., Nowell M.A., Björnsson B.T., Einarsdottir I.E., Canario A.V.M., and Sweeney G.E. Thyroid hormones in growth and development of fish. Comparative Biochemistry and Physiology 130 (2001) 447-459
Raine J.C. Ontogeny of thyroid function in Rainbouw Trout Oncorhynchus mykiss (1998), The University of Guelph pp. 1-124
Raine J.C., Strelive U., and Leatherland J.F. The thyroid tissue of juvenile Oncorhynchus mykiss is tubular, not follicular. Journal of Fish Biology 67 (2005) 823-833
Rolland R.M. A review of chemically-induced alterations in thyroid and vitamin A status from field studies of wildlife and fish. Journal of Wildlife Diseases 36 (2000) 615-635
Schnitzler J.G. Etude histomorphométrique de la glande thyroïde du marsouin commun (Phocoena phocoena) (L.): Relation potentielle avec différents organohalogénés (2005), Université de liège pp. 1-50
Scholtz A.T., White R.J., Koehler V.A., and Horton S.A. Measurements of Thyroxine concentration as an indicator of the Criticalperiod for Imprinting in Kokanee Salmon (Oncorhynchus nerka): Implications for Operating Lake Roosevelt Kokanee Hatcheries (1992), US Departement of Energy, Portland pp. 88-63, 1-96
Schumacher U., Zahler S., Horny H.-P., Heidemann G., Skirnisson K., and Welsch U. 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 (1993) 103-108
Skaare J.U., Larsen H.J., Lie E., Bernhoft A., Derocher A.E., Norstrom R., Ropstad E., Lunn N.F., and Wiig O. Ecological risk assessment of persistent organic pollutants in the arctic. Toxicology (2002) 193-197
Stamatis N., Ioannidou D., Christoforidis A., and Koutrakis E. Sediment pollution by heavy metals in the Strymonikos and Ierissos Gulfs, North Aegean Sea, Greece. Environmental Monitoring and Assessement 80 (2002) 33-49
Stefanelli P., Ausili A., Di Muccio A., Fossi M.C., Di Muccio S., Rossi S., and Colasanti A. Organochlorine compounds in tissues of swordfish (Xiphias gladius) from Mediterranean Sea and Azores Islands. Marine Pollution Bulletin 49 (2004) 938-950
Storelli M.M., Storelli A., D'Addabbo R., Barone G., and Marcotrigiano G.O. Polychlorinated biphenyl residues in deep-sea fish from Mediterranean Sea. Environment International 30 (2004) 343-349
Sylaios G., Ioannidou D., and Koutrakis E. Water Quality Monitoring in Strymonikos Gulf and Gulf of Ierissos, Northern Greece. In: Brebbia C.A., and Anagnostopoulos P. (Eds). Fifth International conference on water Pollution: Modelling and Prediction vol. 5 (1999), Wit Press 303-310
Thomann R.V., and Connoly J.P. Model of PCB in the lake michigan lake trout food chain. Environmental Science and Technology 18 (1984) 65-71
Wade M., Parent S., Finnson K.W., Foster W., Younglai E., McMahon A., Cyr D.G., and Hughes C. Thyroid toxicity due to subchronic exposure to a complex mixture of 16 Organochlorines, lead and cadmium. Toxicological Sciences 67 (2002) 207-218
Yamano K. The role of thyroid hormone in fish development with reference to aquaculture. JARQ 39 (2005) 161-168
Zhou T., John-Alder H.B., Weis J.S., and Weis P. Endocrine disruption: thyroid dysfunction in mummichogs (Fundulus heteroclitus) from a polluted habitat. Marine Environmental Research 50 (2000) 393-397
Zoeller R.T., Tan S.W., and Tyl R.W. General background on the hypothalamic-pituitary-thyroid (HPT) axis. Critical Reviews in Toxicology 37 (2007) 11-53
