Endocrine Modulation in Atlantic Cod (Gadus morhua L.) Exposed to Alkylphenols, Polyaromatic Hydrocarbons, Produced Water, and Dispersed Oil

Effluent from oil production activities contains chemicals that are suspected of inducing endocrine disruption in fish. In this study, Atlantic cod (Gadus morhua L.) were exposed to mixtures of low- and medium-molecular-weight alkylphenols (AP) (methyl- to heptylphenol), polycyclic aromatic hydrocarbons (PAH), diluted produced water, and dispersed oil for 15 d in a flow-through exposure system. Condition index (CI), hepatosomatic index (HSI), gonadosomatic index (GSI), concentration of the estrogenic biomarker vitellogenin (Vtg), and modulation of the total sex steroid-binding capacity in plasma were determined to assess whether these mixtures were capable of interfering with endocrine-regulated physiological processes in Atlantic cod. No marked differences in plasma Vtg levels were found between control and exposed groups of either males or females, possibly due to high intergroup variances and low sample numbers. An apparent numerical increase in the number of male and female fish with high plasma Vtg levels was, however, observed in some exposure groups compared to control. This purported weak estrogenic effect was several orders of magnitude lower than that observed for potent estrogens and suggested that the levels of estrogen receptor (ER) agonists were low. Exposure of female fish to a mixture of dispersed oil and a mixture of AP, PAH, and dispersed oil led to upregulation of the plasma total sex steroid-binding capacity, indicating interference with the normal blood steroid transport. No significant effects were seen for CI, HSI, and GSI, suggesting that the endocrine-disrupting potential was not sufficient to elicit effects on general physiological conditions and gonad development during this short exposure period.

[1]  K. Tollefsen,et al.  Partial characterization of a sex steroid-binding protein in plasma from arctic charr (Salvelinus alpinus L.). , 2001, General and comparative endocrinology.

[2]  J. Beyer,et al.  Development of a laboratory exposure system using marine fish to carry out realistic effect studies with produced water discharged from offshore oil production. , 2009, Marine pollution bulletin.

[3]  J. Sumpter Endocrine Disrupters in the Aquatic Environment: An Overview , 2005 .

[4]  K. Tollefsen,et al.  Binding of alkylphenols and alkylated non-phenolics to rainbow trout (Oncorhynchus mykiss) hepatic estrogen receptors. , 2008, Ecotoxicology and environmental safety.

[5]  U. Westphal Sex Steroid-Binding Protein (SBP) , 1986 .

[6]  Thierry Baussant,et al.  Bioconcentration, biotransformation, and elimination of polycyclic aromatic hydrocarbons in sheepshead minnows (Cyprinodon variegatus) Exposed to Contaminated Seawater , 2004, Environmental toxicology and chemistry.

[7]  N. Bache,et al.  Biomarker candidate discovery in Atlantic cod (Gadus morhua) continuously exposed to North Sea produced water from egg to fry. , 2010, Aquatic toxicology.

[8]  K. Tollefsen Binding of alkylphenols and alkylated non-phenolics to the rainbow trout (Oncorhynchus mykiss) plasma sex steroid-binding protein. , 2007, Ecotoxicology and environmental safety.

[9]  S. Boitsov,et al.  Gas chromatography-mass spectrometry analysis of alkylphenols in produced water from offshore oil installations as pentafluorobenzoate derivatives. , 2004, Journal of chromatography. A.

[10]  K. Tollefsen Interaction of estrogen mimics, singly and in combination, with plasma sex steroid-binding proteins in rainbow trout (Oncorhynchus mykiss). , 2002, Aquatic toxicology.

[11]  S. Sanni,et al.  A Continuous Flow System (CFS) for chronic exposure of aquatic organisms , 1998 .

[12]  Weida Tong,et al.  Study of 202 natural, synthetic, and environmental chemicals for binding to the androgen receptor. , 2003, Chemical research in toxicology.

[13]  K. Tollefsen,et al.  Assessing combined toxicity of estrogen receptor agonists in a primary culture of rainbow trout (Oncorhynchus mykiss) hepatocytes. , 2011, Aquatic toxicology.

[14]  John P. Sumpter,et al.  Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals , 1996 .

[15]  U. Westphal Steroid-Protein Interactions II , 1986, Monographs on Endocrinology.

[16]  K. Tollefsen,et al.  Environmental estrogens interact with and modulate the properties of plasma sex steroid-binding proteins in juvenile Atlantic salmon (Salmo salar). , 2002, Marine environmental research.

[17]  K. Tollefsen,et al.  Estrogen mimics bind with similar affinity and specificity to the hepatic estrogen receptor in Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). , 2002, General and comparative endocrinology.

[18]  A. Goksøyr,et al.  Candidate biomarker discovery in plasma of juvenile cod (Gadus morhua) exposed to crude North Sea oil, alkyl phenols and polycyclic aromatic hydrocarbons (PAHs). , 2009, Marine environmental research.

[19]  J. Sumpter,et al.  Increase of Plasma Vitellogenin Concentration in Rainbow Trout (Oncorhynchus mykiss) Exposed to Effluents from Oil Refinery Treatment Works and Municipal Sewage , 1997, Bulletin of environmental contamination and toxicology.

[20]  K. Tollefsen,et al.  Estrogenicity of alkylphenols and alkylated non-phenolics in a rainbow trout (Oncorhynchus mykiss) primary hepatocyte culture. , 2008, Ecotoxicology and environmental safety.

[21]  Ketil Hylland,et al.  Water column monitoring near oil installations in the North Sea 2001-2004. , 2008, Marine pollution bulletin.

[22]  K. Morohashi Endocrine disrupters , 1999, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[23]  K. Tollefsen,et al.  Binding of xenoestrogens to the sex steroid-binding protein in plasma from Arctic charr (Salvelinus alpinus L.). , 2004, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[24]  Ståle Johnsen,et al.  Discharges of Produced Water to the North Sea , 1996 .

[25]  P. Thomas,et al.  Partial characterization of a sex-steroid binding protein in the spotted seatrout (Cynoscion nebulosus). , 1994, Biology of reproduction.

[26]  J. Sumpter,et al.  Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. , 1995, Environmental health perspectives.

[27]  S. Holm,et al.  Effects of pulp and paper mill effluents on reproductive success of largemouth bass , 2003, Environmental toxicology and chemistry.

[28]  J. Sumpter Feminized responses in fish to environmental estrogens. , 1995, Toxicology letters.

[29]  K. Tollefsen,et al.  Effluents from oil production activities contain chemicals that interfere with normal function of intra- and extra-cellular estrogen binding proteins. , 2006, Marine environmental research.

[30]  Toril I. Røe Utvik,et al.  Chemical characterisation of produced water from four offshore oil production platforms in the North Sea , 1999 .

[31]  W. Waller,et al.  Assessment of the estrogenicity and toxicity of a domestic wastewater effluent flowing through a constructed wetland system using biomarkers in male fathead minnows (Pimephales promelas rafinesque, 1820) , 2001, Environmental Toxicology and Chemistry.

[32]  K. Tollefsen,et al.  Estrogen receptor (ER) agonists and androgen receptor (AR) antagonists in effluents from Norwegian North Sea oil production platforms. , 2007, Marine pollution bulletin.

[33]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[34]  J. Sumpter,et al.  The dynamics of vitellogenin sequestration into vitellogenic ovarian follicles of the rainbow trout, Salmo gairdneri , 1990, Fish Physiology and Biochemistry.

[35]  H. Leffers,et al.  Comparison of short-term estrogenicity tests for identification of hormone-disrupting chemicals. , 1999 .

[36]  K. Tollefsen,et al.  Effect-directed identification of naphthenic acids as important in vitro xeno-estrogens and anti-androgens in North sea offshore produced water discharges. , 2009, Environmental science & technology.

[37]  A. Svardal,et al.  Effects of alkylphenols on the reproductive system of Atlantic cod (Gadus morhua). , 2007, Aquatic toxicology.