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Endocrine Disruption in the European Eel, Anguilla anguilla, Exposed to an Environmental Cocaine Concentration

Water, Air, & Soil Pollution volume 224, Article number: 1579 (2013) Cite this article

Abstract

The aim of the present study was to verify if cocaine, at environmental concentrations, influences the endocrine system of the European eel. Silver eels (a stage of the eel life cycle preparing the fish for the oceanic reproductive migration) were exposed to a nominal cocaine concentration of 20 ng/l during 30 days; at the same time, control, carrier, and postexposure recovery groups were made. The effects of cocaine were observed in (1) brain dopamine content, (2) plasma catecholamine levels (dopamine, norepinephrine, and epinephrine), (3) pituitary–adrenal axis activity [plasma adrenocorticotropic hormone (ACTH), corticosterone, cortisol, and aldosterone levels], and (4) pituitary–thyroid axis activity [plasma thyroid-stimulating hormone (TSH), triiodothyronine, and thyroxine levels]. In the treated group, brain dopamine, plasma catecholamines, cortisol, and TSH levels were higher, whereas ACTH, corticosterone, and triiodothyronine levels were lower than controls. In the postexposure recovery group, brain dopamine, plasma dopamine and epinephrine, and thyroxine levels further increased, whereas plasma norepinephrine, cortisol, and corticosterone levels were similar to treated values. Finally, ACTH and TSH were similar, whereas triiodothyronine levels were lower than controls. Aldosterone levels were unaffected by cocaine exposure. The results of the present study show that cocaine, at environmental concentrations, behaves like an endocrine disruptor changing brain dopamine and plasma catecholamine levels and the activity of pituitary–adrenal/thyroid axes. Since the endocrine system plays a key role in the metabolic and reproductive processes of the eel, our results suggest that environmental cocaine could be considered another cause for the decline in the European eel.

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References

  • Andreoletti, G. E., Vellano, C., Colucci, D., Androne, C., Mazzi, V., & Fasolo, A. (1988). Anatomical organization of CRF- and AVT-like systems in the newt hypothalamus and the effects of localized lesion to the posterior hypothalamus on serum aldosterone and corticosterone. Bollettino di Zoologia, 55, 261–268.

    Article  Google Scholar 

  • Baumann, M. H., Gendron, T. M., Becketts, K. M., Henningfield, J. E., Gorelick, D. A., & Rothman, R. B. (1995). Effects of intravenous cocaine on plasma cortisol and prolactin in human cocaine abusers. Biological Psychiatry, 38, 751–755.

    Article  CAS  Google Scholar 

  • Belpaire, C., & Goemans, G. (2007). The European eel Anguilla anguilla, a rapporteur of the chemical status for the water framework directive? Vie et Milieu-Life and Environment, 57, 235–252.

    Google Scholar 

  • Bernier, N. J., & Perry, S. F. (1996). Control of catecholamine and serotonin release from the chromaffin tissue of the Atlantic hagfish. Journal of Experimental Biology, 199, 2485–2497.

    CAS  Google Scholar 

  • Bettinetti, R., Galassi, S., Quadroni, S., Volta, P., Capoccioni, F., Ciccotti, E., et al. (2011). Use of Anguilla anguilla for biomonitoring persistent organic pollutants (POPs) in brackish and riverine waters in central and southern Italy. Water, Air, and Soil Pollution, 217, 321–331.

    Article  CAS  Google Scholar 

  • Borowsky, B., & Kuhn, C. M. (1991). Monoamine mediation of cocaine-induced hypothalamo-pituitary-adrenal activation. Journal of Pharmacology and Experimental Therapeutics, 256, 204–210.

    CAS  Google Scholar 

  • Brecher, E. M., & the editors of Consumer Reports. (1972). Licit and illicit drugs: the consumers union report on narcotics, stimulants, depressants, inhalants, hallucinogens, and marijuana, including caffeine, nicotine, and alcohol. Boston: Little, Brown and Company.

    Google Scholar 

  • Brown, C. L., Doroshov, S. L., Cochran, M. D., & Bern, H. A. (1989). Enhanced survival in swiped bass fingerlings after maternal triiodothyronine treatment. Fish Physiology and Biochemistry, 7, 295–299.

    Article  CAS  Google Scholar 

  • Budziszewska, B., Jaworska-Feil, L., & Lasoń, W. (1996). The effect of repeated amphetamine and cocaine administration on adrenal, gonadal and thyroid hormone levels in the rat plasma. Experimental and Clinical Endocrinology & Diabetes, 104(4), 334–338.

    Article  CAS  Google Scholar 

  • Buet, A., Banas, D., Vollaire, Y., Coulet, E., & Roche, H. (2006). Biomarker responses in European eel (Anguilla anguilla) exposed to persistent organic pollutants. A field study in the Vaccarès lagoon (Camargue, France). Chemosphere, 65, 1846–1858.

    Article  CAS  Google Scholar 

  • Capaldo, A., Gay, F., De Falco, M., Virgilio, F., Valiante, S., Laforgia, V., et al. (2006). The newt Triturus carnifex as a model for monitoring the ecotoxic impact of the fungicide thiophanate methyl: adverse effects on the adrenal gland. Comparative Biochemistry and Physiologyt C, 143, 86–93.

    Google Scholar 

  • Capaldo, A., Gay, F., Maddaloni, M., Valiante, S., De Falco, M., Lenzi, M., et al. (2012). Presence of cocaine in the tissues of the European eel, Anguilla anguilla, exposed to environmental cocaine concentrations. Water, Air, and Soil Pollution, 223, 2137–2143.

    Article  CAS  Google Scholar 

  • Castiglioni, S., Zuccato, E., Crisci, E., Chiabrando, C., Fanelli, R., & Bagnati, R. (2006). Identification and measurement of illicit drugs and their metabolites in urban wastewater by liquid chromatography-tandem mass spectrometry. Analytical Chemistry, 78, 8421–8429.

    Article  CAS  Google Scholar 

  • Chiueh, C. C., & Kopin, I. J. (1978). Centrally mediated release by cocaine of endogenous epinephrine and norepinephrine from the sympathoadrenal medullary system of unanesthetized rats. Journal of Pharmacology and Experimental Therapeutics, 205, 148–154.

    CAS  Google Scholar 

  • Cyr, D. G., & Eales, J. G. (1988). In vitro effects of thyroid hormones on gonadotropin-induced estradiol-17β, secretion by ovarian follicles of rainbow trout, Salmo gairdneri. General and Comparative Endocrinology, 69, 80–87.

    Article  CAS  Google Scholar 

  • Daughton, C. G. (2011). Illicit drugs: contaminants in the environment and utility in forensic epidemiology. In D. M. Whitacre (Ed.), Reviews of environmental contamination and toxicology (pp. 59–110). New York: Springer.

    Google Scholar 

  • de Boer, J., Dao, Q. T., van Leeuwen, S. P. J., Kotterman, M. J. J., & Schobben, J. H. M. (2010). Thirty year monitoring of PCBs, organochlorine pesticides and tetrabromodiphenylether in eel from The Netherlands. Environmental Pollution, 158, 1228–1236.

    Article  Google Scholar 

  • Dhopesh, V. P., Burke, W. M., Maany, I., & Ravi, N. V. (1991). Effect of cocaine on thyroid functions. The American Journal of Drug and Alcohol Abuse, 17, 423–427.

    Article  CAS  Google Scholar 

  • Dickoff, W. W., Yan, L., Plisetskaya, E. M., Sullivan, C. V., Swanson, P., Hara, A., et al. (1989). Relationship between metabolic and reproductive hormones in salmonid fish. Fish Physiology and Biochemistry, 7, 147–155.

    Article  Google Scholar 

  • Donnè Schmidt, E., Tilders, F. J. H., Janszen, A. W. J. W., Binnekade, R., De Vries, T., & Schoffelmeer, A. N. M. (1995). Intermittent cocaine exposure causes delayed and long-lasting sensitization of cocaine-induced ACTH secretion in rats. European Journal of Pharmacology, 285, 317–321.

    Article  Google Scholar 

  • Dufour, S., Burzawa-Gérard, E., Le Belle, N., Sbaihi, M., & Vidal, B. (2003). Reproductive endocrinology of the European eel, Anguilla anguilla. In K. Aida, K. Tsukamoto, & K. Yamauchi (Eds.), Eel Biology (pp. 373–383). Tokyo: Springer.

    Chapter  Google Scholar 

  • Dufour, S., Weltzien, F. A., Sebert, M. E., Le Belle, N., Vidal, B., Vernier, P., et al. (2005). Dopaminergic inhibition of reproduction in teleost fishes. Ecophysiological and evolutionary implications. Annals of the New York Academy of Sciences, 1040, 9–21.

    Article  CAS  Google Scholar 

  • Dufour, S., Sebert, M. E., Weltzein, F. A., Rousseau, K., & Pasqualini, C. (2010). Neuroendocrine control by dopamine of teleost reproduction. Journal of Fish Biology, 76, 129–160.

    Article  CAS  Google Scholar 

  • Fabbri, E., Capuzzo, A., & Moon, T. W. (1998). The role of circulating catecholamines in the regulation of fish metabolism: an overview. Comparative Biochemistry and Physiology. C, 120, 177–192.

    CAS  Google Scholar 

  • Goldstein, R. A., DesLauriers, C., & Burda, A. M. (2009). Cocaine: history, social implications, and toxicity—a review. Seminars in Diagnostic Pathology, 26, 10–17.

    Article  Google Scholar 

  • Goletiani, N. V., Mendelson, J. H., Sholar, M. B., Siegel, A. J., & Mello, N. K. (2009). Opioid and cocaine combined effects on cocaine-induced changes in HPA and HPG axes hormones in men. Pharmacology Biochemistry and Behavior, 91, 526–536.

    Article  CAS  Google Scholar 

  • Heberer, T. (2002). Occurrence, fate, and removal of pharmaceuticals residues in the aquatic environment: a review of recent research data. Toxicology Letters, 131, 5–17.

    Article  CAS  Google Scholar 

  • Hontela, A., Dumont, P., Duclos, D., & Jean Fortin, R. E. (1995). Endocrine and metabolic dysfunction in yellow perch, Perca flavescens, exposed to organic contaminants and heavy metals in the St. Lawrence River. Environmental Toxicology and Chemistry, 14, 725–731.

    CAS  Google Scholar 

  • Kalivas, P. W., & Volkow, N. D. (2005). The neural basis of addiction: a pathology of motivation and choice. The American Journal of Psychiatry, 162, 1403–1413.

    Article  Google Scholar 

  • Levy, A. D., Li, Q., Alvarez Sanz, M. C., Brownfield, M. S., & Van de Kar, L. D. (1992). Repeated cocaine modifies the neuroendocrine responses to the 5-HT1C/5-HT2 receptor agonist DOI. European Journal of Pharmacology, 221, 121–127.

    Article  CAS  Google Scholar 

  • Lim, E. K., & Peters, T. J. (1984). Ammonium acetate: a general purpose buffer for clinical applications of high-performance liquid chromatography. Journal of Chromatography, 316, 397–406.

    Article  CAS  Google Scholar 

  • Lòpez-Patiño, M. A., Yu, L., Cabral, H., & Zhdanova, I. V. (2008a). Anxiogenic effects of cocaine withdrawal in zebrafish. Physiology & Behavior, 93, 160–171.

    Article  Google Scholar 

  • Lòpez-Patiño, M. A., Yu, L., Yamamoto, B. K., & Zhdanova, I. V. (2008b). Gender differences in zebrafish responses to cocaine withdrawal. Physiology & Behavior, 95, 36–47.

    Article  Google Scholar 

  • Mari, F., Politi, L., Biggeri, A., Accetta, G., Trignano, C., Di Padua, M., et al. (2009). Cocaine and heroin in waste water plants: a 1-year study in the city of Florence, Italy. Forensic Science International, 189, 88–92.

    Article  CAS  Google Scholar 

  • Martin, B. J., Naughton, B. J., Thirtamara-Rajamani, K., Yoon, D. J., Han, D. D., Devries, A. C., et al. (2011). Dopamine transporter inhibition is necessary for cocaine-induced increases in dendritic spine density in the nucleus accumbens. Synapse, 65, 490–496.

    Article  CAS  Google Scholar 

  • McClung, C., & Hirsh, J. (1998). Stereotypic behavioral responses to free-base cocaine and the development of behavioral sensitization in Drosophila. Current Biology, 8, 109–112.

    Article  CAS  Google Scholar 

  • Mendelson, J. H., Teoh, S. K., Mello, N. K., Ellingboe, J., & Rhoades, E. (1992). Acute effects of cocaine on plasma adrenocorticotropic hormone, luteinizing hormone and prolactin levels in cocaine-dependent men. Journal of Pharmacology and Experimental Therapeutics, 263, 505–509.

    CAS  Google Scholar 

  • Nestler, E. J., & Malenka, R. C. (2004). The addicted brain. Scientific American, 290, 78–85.

    Article  CAS  Google Scholar 

  • Nilsson, S. (1983). Autonomic nerve function in the vertebrates. Berlin: Springer.

    Book  Google Scholar 

  • Norris, D.O. (2007). Vertebrate endocrinology. Amsterdam: Academic.

  • Pal, R., Megharaj, M., Kirkbride, K. P., & Naidu, R. (2012). Illicit drugs and the environment—a review. Science of the Total Environment. doi:10.1016/j.scitotenv.2012.05.086.

    Google Scholar 

  • Pasqualini, C., Weltzien, F. A., Vidal, B., Baloche, S., Rouget, C., Gilles, N., et al. (2009). Two distinct dopamine D2 receptor genes in the European eel: molecular characterization, tissue-specific transcription, and regulation by sex steroids. Endocrinology, 150, 1377–1392.

    Article  CAS  Google Scholar 

  • Perry, S. F., & Capaldo, A. (2011). The autonomic nervous system and chromaffin tissue: neuroendocrine regulation of catecholamine secretion in non-mammalian vertebrates. Autonomic Neuroscience: Basic and Clinical, 165, 54–66.

    Article  CAS  Google Scholar 

  • Perry, S. F., Fritsche, R., & Thomas, S. (1993). Storage and release of catecholamines from the chromaffin tissue of Atlantic hagfish, Myxine glutinosa. The Journal of Experimental Biology, 183, 165–184.

    CAS  Google Scholar 

  • Perry, S. F., Kinkead, R., & Fritsche, R. (1992). Are circulating catecholamines involved in the control of breathing by fishes? Reviews in Fish Biology and Fisheries, 2, 65–83.

    Article  Google Scholar 

  • Perry, S. F., & Wood, C. M. (1989). Control and coordination of gas transfer in fishes. Canadian Journal of Zoology, 67, 2961–2970.

    Article  Google Scholar 

  • Postigo, C., de Alda, M. J. L., & Barcelò, D. (2010). Drugs of abuse and their metabolites in the Ebro river basin: occurrence in sewage and surface water, sewage treatment plants removal efficiency, and collective drug usage estimation. Environment International, 36, 75–84.

    Article  CAS  Google Scholar 

  • Redding, J. M., DeLuze, A., Leloup-Hatey, J., & Leloup, J. (1986). Suppression of plasma thyroid hormone concentrations by cortisol in the European eel Anguilla anguilla. Comparative Biochemistry and Physiology. Part A, Physiology, 83, 409–413.

    Article  CAS  Google Scholar 

  • Rehm, J., Taylor, B., & Room, R. (2006). Global burden of disease from alcohol, illicit drugs and tobacco. Drug and Alcohol Review, 25, 503–513.

    Article  Google Scholar 

  • Robinet, T., & Feunteun, E. (2002). Sublethal effects of exposure to chemical compounds: a cause for the decline in Atlantic eels? Ecotoxicology, 11, 265–277.

    Article  CAS  Google Scholar 

  • Schwartz, A. B., Boyle, W., Janzen, D., & Jones, R. T. (1988). Acute effects of cocaine on catecholamines and cardiac electrophysiology in the conscious dog. The Canadian Journal of Cardiology, 4, 188–192.

    CAS  Google Scholar 

  • Sciarrillo, R., De Falco, M., Virgilio, F., Laforgia, V., Capaldo, A., Gay, F., et al. (2008). Morphological and functional changes in the thyroid gland of methyl thiophanate-injected lizards, Podarcis sicula. Archives of Environmental Contamination and Toxicology, 55, 254–261.

    Article  CAS  Google Scholar 

  • Sébert, M. E., Weltzien, F. A., Moisan, C., Pasqualini, C., & Dufour, S. (2008). Dopaminergic systems in the European eel: characterization, brain distribution, and potential role in migration and reproduction. Hydrobiologia, 602, 27–46.

    Article  Google Scholar 

  • Shelby-Walker, J. A., Ward, C. K., & Mendonça, M. T. (2009). Reproductive parameters in female yellow-blotched map turtles (Graptemys flavimaculata) from a historically contaminated site vs. a reference site. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 154(3), 401–408.

    Article  Google Scholar 

  • Sofuoglu, M., Nelson, D., Babb, D. A., & Hatsukami, D. K. (2001). Intravenous cocaine increases plasma epinephrine and norepinephrine in humans. Pharmacology Biochemistry and Behavior, 68, 455–459.

    Article  CAS  Google Scholar 

  • Terlizzi, A., Geraci, S., & Minganti, V. (1998). Tributyltin (TBT) pollution in the coastal waters of Italy as indicated by imposex in Hexaplex trunculus (Gastropoda, Muricidae). Marine Pollution Bulletin, 36, 749–752.

    Article  CAS  Google Scholar 

  • Van Anholt, R. D., Spanings, T., Koven, W., & Wendelar Bonga, S. E. (2003). Effects of acetylsalicylic acid treatment on thyroid hormones, prolactins, and the stress response of tilapia (Oreochromis mossambicus). American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 285, R1098–R1106.

    Google Scholar 

  • van Ginneken, V., Palstra, A., Leonards, P., Nieveen, M., van den Berg, H., Flik, G., et al. (2009). PCBs and the energy cost of migration in the European eel (Anguilla Anguilla L.). Aquatic Toxicology, 92, 213–220.

    Article  Google Scholar 

  • Van Waarde, G., van den Thillart, G., & Kesbeke, F. (1983). Anaerobic energy metabolism of the European eel Anguilla anguilla. Journal of Comparative Physiology, 149, 469–475.

    Google Scholar 

  • Vidal, B., Pasqualini, C., Le Belle, N., Holland, M. C. H., Sbaihi, M., Vernier, P., et al. (2004). Dopamine inhibits luteinizing hormone synthesis and release in the juvenile European eel: a neuroendocrine lock for the onset of puberty. Biology of Reproduction, 71, 1491–1500.

    Article  CAS  Google Scholar 

  • Weber, G. W., Okimoto, D. K., Richman, N. H., & Grau, E. G. (1992). Patterns of thyroxine and triiodothyronine in serum and follicle-bound oocytes of the tilapia, Oreochromis mossambicus during oogenesis. General and Comparative Endocrinology, 85(3), 392–404.

    Article  CAS  Google Scholar 

  • Zizza, M., Giusi, G., Crudo, M., Canonaco, M., & Facciolo, R. M. (2012). Lead-induced neurodegenerative events and abnormal behaviors occur via ORXRergic/GABA(A)Rergic mechanisms in a marine teleost. Aquatic Toxicology, 126C, 231–241.

    Google Scholar 

  • Zuccato, E., & Castiglioni, S. (2009). Illicit drugs in the environment. Philosophical Transactions of the Royal Society A, 367, 3965–3978.

    Article  CAS  Google Scholar 

  • Zuccato, E., Castiglioni, S., Bagnati, R., Chiabrando, C., Grassi, P., & Fanelli, R. (2008). Illicit drugs, a novel group of environmental contaminants. Water Research, 42, 961–968.

    Article  CAS  Google Scholar 

  • Zuccato, E., Chiabrando, C., Castiglioni, S., Calamari, D., Bagnati, R., Schiarea, S., et al. (2005). Cocaine in surface waters: a new evidence-based tool to monitor community drug abuse. Environmental Health: a Global Access Science Source, 4, 14–21.

    Google Scholar 

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Acknowledgments

The authors would like to dedicate this paper to the memory of a dear friend and famous endocrinologist, Prof. Tullio Criscuolo, for his loving and constant help in their work.

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  1. Department of Biology, University Federico II, Via Mezzocannone 8, 80134, Naples, Italy

    Flaminia Gay, Massimo Maddaloni, Salvatore Valiante, Vincenza Laforgia & Anna Capaldo

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  1. Flaminia Gay
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  2. Massimo Maddaloni
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  3. Salvatore Valiante
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  4. Vincenza Laforgia
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Correspondence to Anna Capaldo.

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Gay, F., Maddaloni, M., Valiante, S. et al. Endocrine Disruption in the European Eel, Anguilla anguilla, Exposed to an Environmental Cocaine Concentration. Water Air Soil Pollut 224, 1579 (2013). https://doi.org/10.1007/s11270-013-1579-0

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Keywords

  • Anguilla anguilla
  • Cocaine and eel catecholamines
  • Cocaine and eel corticosteroids
  • Cocaine and eel thyroid hormones
  • Eel endocrine disruption