Acute Effects of Tetracycline Exposure in the Freshwater Fish Gambusia holbrooki: Antioxidant Effects, Neurotoxicity and Histological Alterations

Archives of Environmental Contamination and Toxicology

Volumn 68, Issue 2, 2015, Pages 371-381

  Nunes, B ^a,b   Antunes, S C ^b,c   Gomes, R ^d   Campos, J C ^d   Braga, M R ^d   Ramos, A S ^c   Correia, A T ^a,d  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSIDADE FERNANDO PESSOA   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINESTERASE; ANTIOXIDANT; CATALASE; GLUTATHIONE TRANSFERASE; LIPID; TETRACYCLINE; ANTIINFECTIVE AGENT; FRESH WATER; WATER POLLUTANT;

ANTIBIOTICS; ANTIOXIDANT; AQUACULTURE; BIOMONITORING; DEFENSE MECHANISM; ECOTOXICOLOGY; ENZYME ACTIVITY; FRESHWATER ECOSYSTEM; HISTOLOGY; LIVESTOCK; NONTARGET ORGANISM; POLLUTION EFFECT; POLLUTION EXPOSURE; TELEOST;

ACUTE TOXICITY; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EXPOSURE; ECOTOXICOLOGY; ENZYME ACTIVITY; FEMALE; GAMBUSIA HOLBROOKI; GILL; HISTOPATHOLOGY; LIVER; MALE; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; ANIMAL; CHEMISTRY; CYPRINODONTIFORMES; METABOLISM; TOXICITY; WATER POLLUTANT;

GAMBUSIA HOLBROOKI;

ANIMALS; ANTI-BACTERIAL AGENTS; CATALASE; CYPRINODONTIFORMES; FRESH WATER; GLUTATHIONE TRANSFERASE; TETRACYCLINE; WATER POLLUTANTS, CHEMICAL;

EID: 84927172869     PISSN: 00904341     EISSN: 14320703     Source Type: Journal    
DOI: 10.1007/s00244-014-0101-z     Document Type: Article

References (82)

1. Aebi H (1984) Catalase in vitro. Methods Enzymol 6:105-121
2. Alazemi BM, Lewis JW, Andrews EB (1996) Gill damage in the fresh water fish Gnathonemus petersii (family: Mormyridae) exposed to selected pollutants: an ultrastructural study. Environ Technol 17(3):225-238
3. Amacher DE, Martin BA (1997) Tetracycline-induced steatosis in primary canine hepatocyte cultures. Fundam App Toxicol 40(2):256-263
4. Asha KK, Sankar TV, Nair PGV (2007) Effect of tetracycline on pancreas and liver function of adult male albino rats. J Pharmacy Pharmacol 59:1241-1248
5. Barceló D (2003) Emerging pollutants in water analysis. Trends Anal Chem 22(10):15-16
6. Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22(1):25-34
7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
8. Brunelli E, Mauceri A, Maisano M, Bernabo I, Giannetto A, De Domenico E et al (2011) Ultrastructural and immunohistochemical investigation on the gills of the teleost, Thalassoma pavo L., exposed to cadmium. Acta Histochem 113:201-213
9. Bruno DW (1989) An investigation into oxytetracycline residues in Atlantic salmon, Salmo salar L. J Fish Dis 12(2):77-86
10. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302-310
11. Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8(7):1137-1144
12. Cabral A, Marques C (1999) Life history, population dynamics and production of eastern mosquito fish, Gambusia holbrooki (Pisces, Poeciliidae) in rice fields of the lower Mondego River Valley, Western Portugal. Acta Oecol 20(6):607-620
13. Camargo MMP, Martinez CBR (2007) Histopathology of gills, kidney and liver of a neotropical fish caged in an urban stream. Neotrop Ichthyol 5(3):327-336
14. Castiglioni S, Bagnati R, Calamari D, Fanelli R, Zuccato E (2005) A multiresidue analytical method using solid-phase extraction and high-pressure chromatography tandem mass spectrometry to measure pharmaceuticals of different therapeutic classes in urban waste waters. J Chromatogr A 1092(2):206-215
15. Cengiz E, Unlu E (2006) Sublethal effects of commercial deltamethrin on the structure of the gill, liver and gut tissues of mosquitofish, Gambusia affinis: a microscopic study. Environ Toxicol Pharmacol 21:246-253
16. Cerqueira MA, Vieira FN, Ferreira RV, Silva JF (2005) The water quality of the Cértima River Basin (Central Portugal). Environ Monit Assess 111:297-306
17. Chambers HF (2001) Cloramphenicol, tetracyclines, macrolides, clindamycin and streptogramins. In: Katzung BG (ed) Basic and clinical pharmacology, 8th edn. McGraw-Hill, New York, pp 774-783
18. Chen WR, Huang CH (2009) Transformation of tetracyclines mediated by Mn(II) and Cu(II) ions in the presence of oxygen. Environ Sci Technol 43(2):401-407
19. Cleuvers M (2003) Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicol Lett 142(3):185-194
20. Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle changes? Environ Health Perspect 107(6):907-938
21. De Domenico E, Mauceri A, Giordano G, Maisano M, Gioffrè G, Natalotto A et al (2011) Effects of "in vivo" exposure to toxic sediments on juveniles of sea bass (Dicentrarchus labrax). Aquat Toxicol 105:688-697
22. De Domenico E, Mauceri A, Giordano D, Maisano M, Giannetto A, Parrino V et al (2013) Biological responses of juvenile European sea bass (Dicentrarchus labrax) exposed to contaminated sediments. Ecotoxicol Environ Saf 97:114-123
23. Deblonde T, Cossu-Leguilla C, Hartemann P (2011) Emerging pollutants in wastewater: a review of the literature. Int J Hyg Environ Health 214:442-448
24. Díaz-Cruz MS, Alda MJL, Barceló D (2003) Environmental behavior and analysis of veterinary and human drugs in soils, sediments and sludge. Trends Anal Chem 22(6):340-351
25. Dong L, Gao J, Xie X, Zhou Q (2012) DNA damage and biochemical toxicity of antibiotics in soil on the earthworm Eisenia fetida. Chemosphere 89(1):44-51
26. Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88-95
27. Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97-177
28. Ezemonye LI, Ikpesu TO (2011) Evaluation of sub-lethal effects of endosulfan on cortisol secretion, glutathione S-transferase and acetylcholinesterase activities in Clarias gariepinus. Food Chem Toxicol 49(9):1898-1903
29. Fatta-Kassinos D, Meric S, Nikolaou A (2011) Pharmaceutical residues in environmental waters and wastewater: current state of knowledge and future research. Anal Bioanal Chem 399:251-275
30. Fernandes MN, Mazon AF (2003) Environmental pollution and fish gill morphology. In: Val AL, Kapoor BG (eds) Fish adaptations. Science, Enfield, pp 203-231
31. Fernandes C, Fontaínhas-Fernandes A, Rocha E, Salgado MA (2008) Monitoring pollution in Esmoriz-Paramos lagoon, Portugal: liver histological and biochemical effects in Liza saliens. Environ Monit Assess 145(1-3):315-322
32. Gravato C, Guimarães L, Santos J, Faria M, Alves A, Guilhermino L (2010) Comparative study about the effects of pollution on glass and yellow ells (Anguilla anguilla) from the estuaries of Minho, Lima and Douro Rivers (NM Portugal). Ecotoxicol Environ Saf 73(4):524-533
33. Gu C, Karthikeyan KG (2005) Interaction of tetracycline with aluminum and iron hydrous oxides. Environ Sci Technol 39(8):2660-2667
34. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases - the first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130-7139
35. Halling-Sorensen B, Nielson BN, Lanzky PF, Ingerslev F, Lutzhoft HCH, Jorgensen SE (1998) Occurrence, fate and effects of pharmaceutical substances in the environment - a review. Chemosphere 36(2):357-393
36. Halling-Sorensen B, Sengelov G, Tjornelund J (2002) Toxicity of teracyclines and tetracycline degradation products to environmentally relevant bacteria, including selected tetracycline-resistant bacteria. Arch Environ Contam Toxicol 44:7-16
37. Hawkins WE, Overstreet RM, Provancha MJ (1984) Effects of space shuttle exhaust plumes on gills of some estuarine fishes: a light and electron microscopic study. Gulf Res Rep 7(4):297-309
38. Hirsch R, Ternes R, Haberer K, Kratz KL (1999) Occurrence of antibiotics in the aquatic environment. Sci Total Environ 225(1-2):109-118
39. Hughes GM, Perry SF (1976) Morphometric study of trout gills: a light-microscope method suitable for the evaluation of pollutant action. J Exp Biol 64:447-460
40. Jia A, Xiao Y, Hu J, Asami M, Kunikane S (2009) Simultaneous determination of tetracyclines and their degradation products in environmental waters by liquid chromatography-electrospray tandem mass spectrometry. J Chromatogr A 1216:4655-4662
41. Jones OAH, Voulvoulis N, Lester JN (2002) Aquatic environmental assessment of the top 25 English prescription pharmaceuticals. Water Res 36(20):5013-5022
42. Kang JJ, Fang H (1997) Polycyclic aromatic hydrocarbons inhibit the activity of acetylcholinesterase purified from electric eel. Biochem Biophys Res Commun 238(2):367-369
43. Kraus RL, Pasieczny R, Lariosa-Willingham K, Turner MS, Jiang A, Trauger JW (2005) Antioxidant properties of minocycline: neuroprotection in an oxidative stress assay and direct radical scavenging activity. J Neurochem 94(3):818-827
44. Kummerer K (2009) Antibiotics in the aquatic environment - a review - part I. Chemosphere 75:417-434
45. Machado ALS, Brandão AAH, da Silva CMOM, da Rocha RF (2003) Influence of tetracycline in the hepatic and renal development of rat's offspring. Braz Ach Biol Technol 46(1):47-51
46. Martinez CBR, Nagae MY, Zaia CTBV, Zaia DAM (2004) Morphological and physiological acute effects of lead in the neotropical fish Prochilodus lineatus. Braz J Biol 64(4):797-807
47. Michael I, Rizzo L, McArdell CS, Manaia CM, Merlin C, Schwartz T et al (2013) Urban wastewater treatment plants as hotspots for the release of antibiotics in the environment: a review. Water Res 47(3):957-995
48. Nero V, Farwell A, Lee LEJ, Van Meer T, MacKinnon MD, Dixon DG (2006) The effects of salinity on naphthenic acid toxicity to yellow perch: gill and liver histopathology. Ecotoxicol Environ Saf 65(2):252-264
49. Nico L, Fuller P (2013) Gambusia holbrooki. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov/queries/Factsheet.aspx?speciesID=849. Accessed: May 4, 2013
50. Nunes B (2011) The use of cholinesterases in ecotoxicology. Rev Environ Contam Toxicol 212:29-59
51. Nunes B, Gaio AR, Carvalho F, Guilhermino L (2008) Behaviour and biomarkers of oxidative stress in Gambusia holbrooki after acute exposure to widely used pharmaceuticals and a detergent. Ecotoxicol Environ Saf 72(2):341-354
52. Olsson PE, Larsson A, Haux C (1996) Influence of seasonal changes in water temperature on cadmium inducibility of hepatic and renal metallothionein in rainbow trout. Mar Environ Res 42:41-44
53. Olurin KB, Olojo EAA, Mbaka GO, Akindele AT (2006) Histopathological responses of the gill and liver tissues of Clarias gariepinus fingerlings to the herbicide, glyphosate. AJB 5:2480-2487
54. Organisation for Economic Co-operation and Development (1992) OECD guidelines for the testing of chemicals, Section 2-fish, early-life stage toxicity test (guideline no. 210). OECD Publishing. doi: 10.1787/9789264070103-en
55. Ozmen M, Ayas Z, Gungurdu A, Ekmekci GF, Yerli S (2008) Ecotoxicological assessment of water pollution in Sariyar Dam Lake, Turkey. Ecotoxicol Environ Safe 70(1):167-173
56. Pari L, Gnanasoundari M (2006) Influence of naringenin on oxytetracyclie mediated oxidative damage in rat liver. Basic Clin Pharmacol Toxicol 98(5):456-461
57. Péry AR, Gust M, Vollat B, Mons R, Ramil M, Fink G et al (2008) Fluoxetine effects assessment on the life cycle of aquatic invertebrates. Chemosphere 73(3):300-304
58. Poleksic V, Mitrovic-Tutundzic V (1994) Fish gills as a monitor of sublethal and chronic effects of pollution. In: Müller R, Lloyd R (eds) Sublethal and chronic effects of pollutants on freshwater fish. Fishing New Books, Oxford
59. Ramos AS, Antunes SC, Gonçalves F, Nunes B (2014) The gooseneck barnacle (Pollicipes pollicipes) as a candidate sentinel species for coastal contamination. Arch Environ Toxicol 66(317-326):1
60. Ribeiro SHM (2012) Estimativa dos benefícios da melhoria na qualidade da água no Cértima Master thesis [in Portugese]. University of Aveiro, Portugal
61. Said AA, Matsuki N, Kasuya Y (1995) Effects of aminoglycoside antibiotics on cholinergic autonomic nervous transmission. Pharmacol Toxicol 76(2):128-132
62. Sarmah AK, Meyer MT, Boxall AB (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65(5):725-759
63. Sayed AEDH, Mekkawy IA, Mahmoud UM (2012) Histopathological alterations in some body organs of adult Clarias gariepinus (Burchell, 1822) exposed to 4-nonylphenol, zoology. In: Garcia MD (ed) zoology. InTech, West Palm Beach, pp 163-184
64. Shabana MB, Ibrahim HM, Khadre SEM, Elemam MG (2012) Influence of rifampicin and tetracycline administration on some biochemical and histological parameters in albino rats. J Basic App Zool 65(5):299-308
65. Snavely SR, Hodges GR (1984) The neurotoxicity of antibacterial agents. Ann Intern Med 101(1):92-104
66. Soory M (2008) A role for non-antimicrobial actions of tetracyclines in combating oxidative stress in periodontal and metabolic diseases: a literature review. Open Dent J 2:5-12
67. Spilovska K, Korabecny J, Kral J, Horova A, Musilek K, Soukup O et al (2013) 7-Methoxytacrine-adamantylamine heterodimers as cholinesterase inhibitors in Alzheimer's disease treatment - synthesis, biological evaluation and molecular modeling studies. Molecules 18:2397-2418
68. Stentiford GD, Longshaw M, Lyons BP, Jones G, Green M, Feist SW (2003) Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants. Mar Environ Res 55(2):137-159
69. Stevens DE (1992) Gill morphometry of the red drum, Sciaenops ocellatus. Fish Physiol Biochem 10(2):169-176
70. Sturve J, Almroth BC, Forlin L (2008) Oxidative stress in rainbow trout (Oncorhynchus mykiss) exposed to sewage treatment plant effluent. Ecotoxicol Environ Safe 70(3):446-452
71. Temmink JHM, Bowmieister PJ, Jong P, van der Berg JHJ (1983) An ultra-structural study of chromate-induced hyperplasia in the gill of rainbow trout, Salmo gairdneri. Aquat Toxicol 4(2):165-179
72. Thomas RJ (1994) Neurotoxicity of antibacterial therapy. South Med J 87(9):869-874
73. Tu HT, Silvestre F, Scippo M-L, Thome J-P, Phuong NT, Kestemont P (2009) Acetylcholinesterase activity as a biomarker of exposure to antibiotics and pesticides in the black tiger shrimp (Penaeus monodon). Ecotoxicol Environ Saf 72(5):1463-1470
74. van den Booggard AE, Stobberingh EE (1999) Antibiotic usage in animals: impact on bacterial resistance and public health. Drugs 58(4):589-607
75. Van Dyk JC, Pieterse GM, Van Vuren JHJ (2007) Histological changes in the liver of Oreochromis mossambicus (Cichlidae) after exposure to cadmium and zinc. Ecotoxicol Environ Safe 66:432-440
76. Van Heerden D, Vosloo A, Nikinmaa M (2004) Effects of short-term, copper exposure on gill structure metallothionein and hypoxia-inducible factor-1a (HIF-1a) levels in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 69:271-280
77. Verlicchi P, Galleti A, Petrovic M, Barceló D (2010) Hospital effluents as a source of emerging pollutants: an overview of micropollutants and sustainable treatment options. J Hydrol 389(3-4):416-428
78. Wang QQ, Yates SR (2008) Laboratory study of oxytetracycline degradation kinetics in animal manure and soil. J Agric Food Chem 56(5):1683-1688
79. Wilson JM, Bunte RM, Anthony J, Carty AJ (2009) Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). J Am Assoc Lab Anim Sci 48(6):785-789
80. Wood CM, Soivio A (1991) Environmental effects on gill function: an introduction. Physiol Zool 64:1-3
81. Yasser AG, Naser MD (2011) Impact of pollutants on fish collected from different parts of Shatt Al-Arab River: a histopathological study. Environ Monit Assess 181(1-4):175-182
82. Yonar ME (2012) The effect of lycopene on oxytetracycline-induced oxidative stress and immunosuppression in rainbow trout (Oncorhynchus mykiss, W.). Fish Shellfish Immunol 32(6):994-1001