Human therapeutic plasma levels of the selective serotonin reuptake inhibitor (SSRI) sertraline decrease serotonin reuptake transporter binding and shelter-seeking behavior in adult male fathead minnows

Environmental Science and Technology

Volumn 46, Issue 4, 2012, Pages 2427-2435

  Valenti, Theodore W ^a,c   Gould, Georgianna G ^b   Berninger, Jason P ^a   Connors, Kristin A ^a   Keele, N Bradley ^a   Prosser, Krista N ^a   Brooks, Bryan W ^a  

^a BAYLOR UNIVERSITY   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUATIC ECOSYSTEMS; DOSIMETRY;

ADVERSE OUTCOMES; AQUATIC LIFE; BEHAVIORAL RESPONSE; BINDING ACTIVITIES; FATHEAD MINNOW; HUMAN THERAPEUTICS; MECHANISTICS; PLASMA LEVELS; SELECTIVE SEROTONIN RE-UPTAKE INHIBITORS; SERTRALINE;

FISH;

SEROTONIN REUPTAKE TRANSPORTER; SEROTONIN TRANSPORTER; SERTRALINE; UNCLASSIFIED DRUG;

ABNORMALITY; ADULT; AQUATIC ECOSYSTEM; BEHAVIORAL RESPONSE; CHEMICAL BINDING; CYPRINID; DRUG; INHIBITOR; PH; PLASMA; POLLUTION EXPOSURE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; DOSIMETRY; DRUG BLOOD LEVEL; DRUG EXPOSURE; IONIZATION; MALE; NONHUMAN; PH; PIMEPHALES PROMELAS;

MAMMALIA; PIMEPHALES PROMELAS; VERTEBRATA;

EID: 84857695721     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es204164b     Document Type: Article

References (70)

1. Daughton, C. G.; Brooks, B. W. Active pharmaceuticals ingredients and aquatic organisms. In Environmental Contaminants in Biota-Interpreting Tissue Concentration, 2nd ed.; CRC Press: Boca Raton, FL. 2011; pp 288-337.
2. Oakes, K. D.; Coors, A.; Escher, B. I.; Fenner, K.; Garric, J.; Gust, M.; Knacker, T.; Küster, A.; Kussatz, C.; Metcalfe, C. D.; Monteiro, S.; Moon, T. W.; Mennigen, J. A.; Parrott, J.; Péry, A. R.; Ramil, M.; Roennefahrt, I.; Tarazona, J. V.; Sánchez-Argüello, P.; Ternes, T. A.; Trudeau, V. L.; Boucard, T.; Van Der Kraak, G. J.; Servos, M. R. Environmental risk assessment for the serotonin re-uptake inhibitor fluoxetine: Case study using the European risk assessment framework. Integr. Environ. Assess. Manage. 2010, 6 (1), 524-539.
3. Schultz, M. M.; Furlong, E. T.; Koplin, D. W.; Werner, S. L.; Schoenfuss, H. L.; Barber, L. B.; Blazer, V. S.; Norris, D. O.; Vajda, A. M. Antidepressant pharmaceuticals in two effluent-impacted U.S. streams: Occurrence and fate in water and sediment and selective uptake in fish neural tissue. Environ. Sci. Technol. 2010, 44 (6), 1918-1925.
4. Metcalfe, C. D.; Chus, S.; Judt, C.; Li, H.; Oakes, K. D.; Serovs, M. R.; Andrews, D. M. Antidepressants and their metabolites in municipal wastewater, and downstream exposure in an urban watershed. Environ. Sci. Chem. 2010, 29 (1), 79-89.
5. Bringolf, R. B.; Heltsley, R. M.; Newton, T. J.; Eads, C. B.; Fraley, S. J.; Shea, D.; Cope, W. G. Environmental occurrence and reproductive effects of the pharmaceutical fluoxetine in native freshwater mussels. Environ. Toxicol. Chem. 2010, 29 (6), 1311-1318.
6. Ramirez, A. J.; Brain, R. A.; O'Donnel, J.; Usenko, S.; Mottaleb, M. A.; Perez-Hurtado, P.; Dobbins, L. L.; Pitts, J.; Snyder, B.; Wathen, J.; Stahl, L.; Brooks, B. W.; Chambliss, C. K. Occurrence of pharmaceuticals and personal care products in fish: Results of a national pilot study in the U.S. Environ. Toxicol. Chem. 2009, 28 (12), 2587-2597.
7. Ramirez, A. J.; Mottaleb, M. A.; Brooks, B. W.; Chambliss, C. K. Analysis of pharmaceuticals in fish using liquid chromatographytandem mass spectrometry. Anal. Chem. 2007, 79 (8), 3155-3163. (Pubitemid 46640539)
8. Chu, S.; Metcalfe, C. D. Analysis of paroxetine, fluoxetine and norfluoxetine in fish tissues using pressurized liquid extraction, mixed mode solid phase extraction cleanup and liquid chromatographytandem mass spectrometry. J. Chromatogr. A 2007, 1163 (1-2), 112-118. (Pubitemid 47247703)
9. Brooks, B. W.; Chambliss, C. K.; Stanley, J. K.; Ramirez, A.; Banks, K. E.; Johnson, R. D.; Lewis, R. J. Determination of select antidepressants in fish from an effluent-dominated stream. Environ. Toxicol. Chem. 2005, 24 (2), 464-469. (Pubitemid 40128355)
10. Frazer, A. Serotonergic and noradrenergic reuptake inhibitors: predictions of clinical effects form in vitro potencies. J. Clin. Psychiatry 2001, 62 (12), 16-23. (Pubitemid 32578703)
11. Owen, M. J.; Morgan, W. N.; Plott, S. J.; Nemeroff, C. B. Neurotransmitter receptor and transporter binding profile of antidepressants and their metabolites. J. Pharmacol. Exp. Ther. 1997, 283 (3), 1305-1322. (Pubitemid 28016506)
12. Scheffel, U.; Kim, S.; Cline, E. J.; Kuhar, M. J. Occupancy of the serotonin transporter by fluoxetine, paroxetine, and sertraline: In vivo studies with [125I]RTI-55. Synapse 1994, 16 (4), 263-268. (Pubitemid 24111525)
13. Dietl, M.; Palacios, J. M. Receptor Autoradiography as a tool for the study of the phylogeny of the basal ganglia. J. Recept. Signal Transduction 1988, 8 (1-4), 521-532.
14. Gunnarsson, L.; Jauhiainen, A.; Kristiansson, E.; Nerman, O.; Larsson, D. G. J. Evolutionary conservation of human drug targets in organisms used for environmental risk assessments. Environ. Sci. Technol. 2008, 42 (15), 5807-5813.
15. Wang, Y.; Takai, R.; Yoshioka, H.; Shirabe, K. Characterization and expression of serotonin transporter genes in zebrafish. Tohoku J. Exp. Med. 2006, 208 (3), 267-74.
16. Gould, G,G.; Brooks, B. W.; Frazer, A. Citalopram binding to serotonin transporter sites in minnow brains. Basic Clin. Pharmacol. 2007, 101 (3), 203-210. (Pubitemid 47256384)
17. Benmansour, S.; Cecchi, M.; Morilak, D. C.; Gerhardt, G. A.; Javors, M. A.; Gould, G. G.; Frazer, A. Effects of chronic antidepressant treatments on serotonin transporter function, density and mRNA level. J. Neurosci. 1999, 19 (23), 10494-10501. (Pubitemid 30228055)
18. Brooks, B. W.; Foran, C. M.; Richards, S. M.; Weston, J.; Turner, P. K.; Stanley, J. K.; Solomon, K. R.; Slattery, M.; La Point, T. W. Aquatic ecotoxicology of fluoxetine. Toxicol. Lett. 2003, 142 (3), 169-183. (Pubitemid 36416609)
19. McDonald, M. D.; Gonzalez, A.; Sloman, K. A. Higher levels of aggression are observed in socially dominant toadfish treated with the selective serotonin reuptake inhibitor, fluoxetine. Comp. Biochem. Phys. C 2011, 153 (1), 107-112.
20. Holmberg, A.; Fogel, J.; Albertsson, E.; Fick, J.; Brown, J. N.; Paxeus, N.; Forlin, L.; Johnsson, J. I.; Larsson, D. G. J. Does waterborne citalopram affect the aggressive and sexual behavior of rainbow trout and guppy? J. Hazard. Mater. 2011, 187 (1-3), 596-599.
21. Valenti, T. W.; Perez-Hurtado, P.; Chambliss, C. K.; Brooks, B. W. Aquatic toxicity of sertraline to Pimephales promelas at environmentally relevant surface water pH. Environ. Toxicol. Chem. 2009, 28 (12), 2685-2694.
22. Painter, M. M.; Buerkley, M. A.; Julius, M. L.; Vajda, A. M.; Norris, D. O.; Barber, L. B.; Furlong, E. T.; Schultz, M. M.; Schoenfuss, H. L. Antidepressants at environmentally relevant concentrations affect predator avoidance behavior of larval fathead minnows (Pimephales promelas). Environ. Toxicol. Chem. 2009, 28 (12), 2677-2684.
23. Kreke, N.; Dietrich, D. R. Physiological endpoints for potential SSRI interactions in fish. Crit. Rev. Toxicol. 2008, 38 (3), 215-247. (Pubitemid 351347978)
24. Gaworecki, K. M.; Klaine, S. J. Behavioral and biochemical responses of hybrid striped bass during and after fluoxetine treatment. Aquat. Toxicol. 2008, 88 (40), 207-213.
25. Stanley, J. K.; Ramirez, A. J.; Chambliss, C. K.; Brooks, B. W. Enantiospecific sublethal effects of the antidepressant fluoxetine to a model aquatic vertebrate and invertebrate. Chemosphere 2007, 69 (1), 6-16.
26. Mennigen, J. A.; Stroud, P.; Zamora, J. M.; Moon, T. W.; Trudeau, V. L. Pharmaceuticals as neuroendocrine disruptors: Lessons learned from fish on Prozac. J. Toxicol. Environ. Health B 2011, 14, 387-412.
27. Mennigen, J. A.; Sassine, J.; Trudeau, V. L.; Moon, T. W. Waterborne fluoxetine disrupts feeding and energy metabolism in the goldfish Carassius auratus. Aquat. Toxicol. 2010, 100 (1), 128-137.
28. Mennigen, J. A.; Lado, W. E.; Zamora, J. M.; Duarte-Guterman, P.; Langlois, V. S.; Metcalfe, C. D.; Chang, J. P.; Moon, T. W.; Trudeau, V. L. Waterborne fluoxetine disrupts the reproductive axis in sexually mature male goldfish Carassius auratus. Aquat. Toxicol. 2010, 100 (4), 354-364.
29. Lister, A.; Regan, C.; Van Zwol, J.; Van Der Kraak, G. Inhibition of egg production in zebrafish by fluoxetine and municipal effluents: A mechanistic evaluation. Aquat. Toxicol. 2009, 95 (4), 320-329.
30. Foran, C. M.; Weston, J.; Slattery, M.; Brooks, B. W.; Huggett, D. B. Reproductive assessment of Japanese medaka (Oryzias latipes) following a four-week fluoxetine (SSRI) exposure. Arch. Environ. Contam. Toxicol. 2004, 46 (4), 511-517. (Pubitemid 38529646)
31. Lajeunesse, A.; Gagnon, C.; Gagne, F.; Louis, S.; Cejka, P.; Sauve, S. Distribution of antidepressants and metabolites in brook trout exposed to municipal wastewaters before and after ozone treatment -Evidence of biological effects. Chemosphere 2011, 83 (4), 564-571.
32. Morando, M. B.; Medeiros, L. R.; McDonald, M. D. Fluoxetine treatment affects nitrogen waste excretion and osmoregulation in a marine teleost fish. Aquat. Toxicol. 2009, 95 (2), 164-171.
33. Ankley, G. T.; Brooks, B. W.; Huggett, D. B.; Sumpter, J. P. Repeating history: Pharmaceuticals in the environment. Environ. Sci. Technol. 2007, 41 (24), 8211-8217. (Pubitemid 350276421)
34. Brooks, B. W.; Huggett, D. B.; Boxall, A. B. A. Pharmaceuticals and personal care products: Research needs for the next decade. Environ. Toxicol. Chem. 2009, 28 (12), 2469-2472.
35. Scott, G. R.; Sloman, K. A. The effects of environmental pollutants on complex fish behavior: Integrating behavioral and physiological indicators of toxicity. Aquat. Toxicol. 2004, 68 (4), 369-392. (Pubitemid 38726150)
36. Kasumyan, A. O. Effects of chemical pollutants on foraging behavior and sensitivity of fish to food stimuli. J. Ichthyol. 2001, 41 (1), 76-87. (Pubitemid 33237365)
37. Sandheinrich, M. B.; Atchison, G. J. Sublethal toxicant effects on fish foraging behavior: Empirical vs. mechanistic approaches. Environ. Toxicol. Chem. 1990, 9 (1), 107-119. (Pubitemid 20158552)
38. Grippo, M. A.; Heath, A. G. The effect of mercury on the feeding behavior of fathead minnows (Pimephales promelas). Ecotoxicol. Environ. Safe. 2003, 55 (20), 187-198. (Pubitemid 36555404)
39. Weis, J. S.; Samson, J.; Zhou, T.; Skurnick, J.; Weis, P. Evaluating prey capture by larval mummichogs (Fundulus heteroclitus) as a potential biomarker for contaminants. Mar. Environ. Res. 2003, 55 (1), 27-38. (Pubitemid 35300103)
40. Martinovic, D.; Hogarth, W. T.; Jones, R. E.; Sorensen, P. W. Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows. Environ. Toxicol. Chem. 2007, 26 (2), 271-278. (Pubitemid 46191368)
41. Perreault, H. A. N.; Semsar, K.; Godwin, J. Fluoxetine treatment decreases territorial aggression in coral reef fish. Physiol. Behav. 2003, 79 (4-5), 719-724. (Pubitemid 37087966)
42. Blaxter, J. H. S.; Hallers-Tjabbes, C. C. T. The effect of pollutants on sensory systems and behaviour of aquatic animals. Neth. J. Aquat. Ecol. 1992, 26 (1), 43-58.
43. Baraban, S. C.; Taylor, M. R.; Castro, P. A.; Baier, H. Pentylenetetrazole induced changes in zebrafish behavior, neural activity, and c-fos expression. Neuroscience 2005, 131 (3), 759-768. (Pubitemid 40261229)
44. Berninger, J. P.; Brooks, B. W. Leveraging mammalian pharmaceutical toxicology and pharmacology data to predict chronic fish responses to pharmaceuticals. Toxicol. Lett. 2010, 193 (1), 69-78.
45. Huggett, D. B.; Cook, J. C.; Ericson, J. F.; Williams, R. T. A theoretical model for utilizing mammalian pharmacological and safety data to prioritize potential impacts of human pharmaceuticals to fish. Hum. Ecol. Risk. Assess. 2003, 9 (7), 1789-1799. (Pubitemid 38571547)
46. Fitzsimmons, P. N.; Fernadez, J. D.; Hoffman, A. D.; Butterworth, B. C.; Nichols, J. W. Branchial elimination of superhydrophobic organic compounds by rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 2001, 5 (1-2), 23-34. (Pubitemid 32884265)
47. Fick, J.; Lindberg, R. H.; Parkkonen, J.; Arvidsson, B.; Tysklind, M.; Larsson, D. G. J. Therapeutic levels of levonorgestrel detected in blood plasma of fish: Results from screening rainbow trout exposed to treated sewage effluents. Environ. Sci. Technol. 2010, 44 (7), 2661-2666.
48. Fick, J.; Lindberg, R. H.; Tysklind, M.; Larsson, D. G. J. Predicted critical environmental concentrations for 500 pharmaceuticals. Regul. Toxicol. Pharmacol. 2010, 58 (3), 516-523.
49. Cuklev, F.; Kristiansson, E.; Fick, J.; Asker, N.; Forlin, L.; Larsson, D. G. J. Diclofenac in fish: Blood plasma levels similar to human therapeutic levels affect global hepatic gene expression. Environ. Toxicol. Chem. 2011, 30 (9), 2126-2134.
50. Ankley, G. T.; Bennett, R. S.; Erickson, R. J.; Hoff, D. J.; Horning, M. W.; Johnson, R. D.; Mount, D. R.; Nichols, J. W.; Russom, C. L.; Schmieder, P. K.; Serrano, J. A.; Tietge, J. E.; Villeneuve, D. L. Adverse outcome pathways: A conceptual framework to support ecotoxicology research and risk assessment. Environ. Toxicol. Chem. 2010, 29 (3), 730-741.
51. Nakamura, Y.; Yamamoto, H.; Sekizawa, J.; Kondo, T.; Hirai, N.; Tatarazako, N. The effects of pH on fluoxetine in Japanese medaka (Oryzias latipes): Acute toxicity in fish larvae and bioaccumulation in juvenile fish. Chemosphere 2008, 70 (5), 865-873. (Pubitemid 350138543)
52. Berninger, J. P.; Du, B.; Conners, K. A.; Eytcheson, S. A.; Kolkmeier, M. A.; Prosser, K. N.; Valenti, T. W.; Chambliss, C. K.; Brooks, B. W. Effects of the antihistamine diphenhydramine on selected aquatic organisms. Environ. Toxicol. Chem. 2011, 30 (9), 2065-2072.
53. Thomson, P. D. R. Physicians' Desk Reference, 62nd ed.; Thomson P.D.R.: Montvale, NJ, 2008; 3482 pp.
54. Gernhardt, A. Aquatic behavioral ecotoxicology-Prospects and limitations. Hum. Ecol. Risk. Assess. 2007, 13 (3), 481-491.
55. Peakall, D. B. Disrupted patterns of behavior in natural populations as an index of ecotoxicity. Environ. Health Perspect. 1996, 104 (Suppl. 2), 331-335. (Pubitemid 26160807)
56. Rendal, C.; Kusk, K. O.; Trapp, S. Optimal choice of pH for toxicity and bioaccumulation studies of ionizing organic chemicals. Environ. Toxicol. Chem. 2011, 30, 2395-2406.
57. Valenti, T. W.; Taylor, J. T.; Back, J. A.; King, R. S.; Brooks, B. W. Influence of drought and total phosphorus on diel pH in wadeable streams: Implications for ecological risk assessment of ionizable contaminants. Integr. Environ. Assess. Manage. 2011, 7, 636-647.
58. Meredith-Williams, M.; Carter, L. J.; Fussell, R.; Raffaelli, D.; Ashauer, R.; Boxall, A. B. A. Uptake and depuration of pharmaceuticals in aquatic invertebrates. Environ. Pollut., 2012, in press.
59. Brausch, J. M.; Connors, K. A.; Brooks, B. W.; Rand, G. M. Human pharmaceuticals in the aquatic environment: A critical review of recent toxicological studies and considerations for toxicity testing. Rev. Environ. Contam. Toxicol. 2012, 218, in press.
60. Homlberg, A.; Fogel, J.; Albertsson, E.; Fick, J.; Brown, J. N.; Paxeus, N.; Forlin, L.; Johnsson, J. I.; Larsson, D. G. J. Does waterborne citalopram affect the aggressive and sexual behaviour of rainbow trout and guppy? J. Hazard. Mater. 2011, 187, 596-599.
61. Daws, L. C. Unfaithful neurotransmitter transporters: Focus on serotonin uptake and implications for antidepressants. Pharmacol. Ther. 2009, 121 (1), 89-99.
62. Maximino, C.; de Brito, M.; de Moraes, F. D.; de Oliveira, F. V. C. A comparative analysis of the preference for dark environments in five teleosts. Int. J. Comp. Psych. 2007, 20, 351-367.
63. Serra, E. L.; Medhalha, C. C.; Mattioli, R. Natural preference of zebrafish (Danio rerio) for a dark environment. Braz. J. Med. Biol. Res. 1999, 32 (12), 1551-1553.
64. Montgomery, K. C. The relationship between fear induced by novel stimulation and exploratory behavior. J. Comp. Physiol. Psychol. 1955, 48 (4), 254-260.
65. Handley, S. L.; McBlane, J. W. An assessment of the elevated Xmaze for studying anxiety and anxiety-modulating drugs. J. Pharmacol. Toxicol. Methods 1993, 29 (3), 129-138. (Pubitemid 23193181)
66. Egan, R. J.; Bergner, C. L.; Hart, P. C.; Cachat, J. M.; Canavello, P. R.; Elegante, M. F.; Elkhayat, S. I.; Bartels, B. K.; Tien, A. K.; Tien, D. H.; Mohnot, S.; Beeson, E.; Glasgow, E.; Amri, H.; Zukowska, Z.; Kalueff, A. V. Understanding behavioural and physiological phenotypes of stress and anxiety in zebrafish. Behav. Brain. Res. 2009, 205 (1), 38-44.
67. Henry, T. B.; Black, M. C. Acute and chronic toxicity of fluoxetine (Selective serotonin reuptake inhibitor) in western mosquitofish. Arch. Environ. Contam. Toxicol. 2008, 54, 325-330.
68. Clements, S.; Schreck, C. B. Chronic administration of fluoxetine alters locomotor behavior, but does not potentiate the locomotor stimulating effects of CRH in juvenile Chinnok salmon (Oncorhynchus tshawytscha). Comp. Biochem. Physiol. 2007, 147 (1), 43-49. (Pubitemid 46467442)
69. Nelson, J. S.; Paetz, M. J. The Fishes of Alberta; University of Alberta Press: Edmonton, Alberta, Canada, 1992.
70. Jamieson, I. Do female fish prefer to spawn in nests with eggs for reasons of mate choice copying or egg survival? Am. Nat. 1995, 145 (5), 824-832.